- Physical activity enhances lean body mass (LBM) in youth and adults.
- LBM growth is underpinned by changes in protein “turn over” that favors the synthesis of new proteins over the breakdown of older ones, which ultimately translates into a positive net protein balance.
- Exercise-induced changes in whole-body protein turnover and net protein balance are qualitatively similar between active children and adults.
- However, the dietary protein-induced enhancement of whole-body net protein balance after exercise is greater in active youth compared with similarly active adults.
- Active youth have a greater sensitivity to dietary amino acids than adults to support the growth and development of LBM.
Childhood and adolescence is characterized by the growth of lean tissues (e.g., muscle and bone) that is unparalleled in adult populations. The complex interplay between physical activity and musculoskeletal health is evident in the direct effect weight-bearing activity has on the growth and mineralization of bone (1). However, physical activity, especially of moderate to vigorous intensity, also promotes the development of lean body (including muscle) mass and muscle strength (2–4), which in turn translates into greater mechanical forces on the musculoskeletal system to enhance physical activity’s osteogenic stimulus (1,5). The positive impact that physical activity has on muscle and bone has led some to suggest that debilitating disorders of aging, such as osteoporosis and sarcopenia, ultimately may be found to have roots in inadequate musculoskeletal development during childhood (6). Therefore, for optimal health, it is essential to adopt an active lifestyle at an early age and throughout the lifespan.
Growth of the musculoskeletal system with age is under the influence of nonmodifiable factors such as genetic predisposition and sex hormones and modifiable environmental factors such as diet and exercise. Provided energy and micronutrient needs are met, dietary protein plays a central role in somatic growth as it provides the substrates (i.e., amino acids) necessary to build muscle and other body proteins. It is well-established in adults that the combined effects of exercise and protein ingestion are essential to enhance muscle and whole-body protein remodeling (reviewed by (7)), which ultimately facilitates the recovery from and adaptation to exercise. However, in contrast to youth who are accumulating lean tissue mass during their normal somatic growth, adults ostensibly only experience a similar “growth” response when initiating a resistance training program. Thus, the present review summarizes the available literature on the effects of exercise and dietary protein ingestion on protein metabolism in active youth and, where possible, contrast them with responses in adults.
Although enhancements in bone growth and muscle development in response to diet and activity may occur indirectly through the hormonal action of somatotrophic axis, focus will be given to the potential direct and more local peripheral effects (e.g., at the muscle level) of dietary protein and exercise in active populations. To standardize the maturational level of youth, biological age will be categorized according to the maturity offset relative to the age of peak height velocity (aPHV) (8). Thus, adolescents will be defined according to a maturity offset of −0.5 to +1.5 of aPHV, which would encompass the pubertal growth spurt, with children below this range. Young adults will be defined as 18–35 yr of age, which is in accordance with the majority of literature in this field and would represent a tapering or complete absence of the pubertal growth spurt (2).
This review hypothesizes that while active youth demonstrate directionally similar changes in whole-body protein metabolism as similarly active adults, their overall anabolic sensitivity to dietary protein and amino acids is enhanced due to the need to support lean tissue growth. This greater anabolic sensitivity manifests as an increased ability to assimilate suboptimal intakes of dietary amino acids into a positive net protein balance in youth. In turn, although youth require relatively more protein per kilogram body mass than adults to support normal somatic growth, the relatively greater meal-protein sensitivity ultimately translates into an attenuated increase in age-specific daily protein requirements for active youth compared with similarly active adults. However, active youth also have a greater net protein balance at an equivalent protein intake, which would help support their normal and exercise-induced augmentation of somatic lean mass growth. Thus, through a combination of a greater sensitivity to dietary amino acids and an increased capacity to build protein mass, it is hypothesized that active youth could be considered “better versions” of adults given their enhanced ability to assimilate dietary protein.
PROTEIN REQUIREMENTS IN ACTIVE YOUTH
General protein requirements in humans typically are defined by the dietary nitrogen intake required to maintain nitrogen balance (NBAL), the assumption being that a net neutral balance (i.e., nitrogen intake equivalent to nitrogen excretion) represents the minimum requirement to maintain “normal” physiological function (9). In contrast to healthy adults, children have distinct nutritional needs due to the importance of dietary protein for the remodeling and development of tissues such as muscle and bone during normal growth. For example, the normal growth velocity of healthy children represents a gain of ~5 cm and ~3 kg per year up to ~10 yr of age, which may further increase by up to threefold during the early pubertal growth spurt and, in the case of lean mass accrual, be enhanced by physical activity (2–4). In addition to the constant increase in body weight during childhood, of which a large proportion is fat-free mass, the composition of lean tissue mass must also “mature” with age as suggested by a reduction in total water content and an increase in protein content (10). Hence, protein requirements in children must not only support basal whole-body protein turnover but also increased rates of protein accretion (i.e., positive NBAL) during growth, which is reflected in their marginally greater protein requirements compared with healthy adults based on NBAL data with an estimated growth factor(i.e., 0.92 vs 0.83 g·kg−1·d−1, respectively) (9). However, it should be noted that recent stable isotope methodology (i.e., the indicator amino acid oxidation (IAAO) technique) suggests that protein requirements might be ~1.6- and ~1.5-fold greater than these NBAL-derived requirements in nonexercising children and adults, respectively (11,12).
It is generally accepted that protein requirements are elevated in active adults as a means to replace amino acid oxidative losses, such as with aerobic-based exercise, and to support the remodeling and growth of lean tissue mass (13). However, the limited research in active children and adolescents makes it difficult to provide strong recommendations as to whether and by how much protein requirements may be elevated in these pediatric populations. Given the potential discordance between NBAL and IAAO methodologies (11,12) as well as the safe intake being determined from a statistical construct (i.e., two SDs above the estimated average requirement (EAR) or the upper 95% confidence interval of the EAR), determining the impact of physical activity on protein requirements is arguably more robust relative to the method-specific EAR. When comparing the available studies estimating protein requirements in active children with the method-specific EAR (i.e., 0.74 and 1.3 g·kg−1·d−1 for NBAL and IAAO, respectively), there is a ~1.4-fold greater requirement than current population-specific recommendations (Fig. 1). This trend also holds true for active adolescents in which the EAR is ~1.5-fold greater than current recommendations. Although these findings could suggest that exercise increases daily protein requirements in active youth, direct comparisons between active and inactive populations within some studies do not support a greater requirement in the active populations (14,17). Thus, the apparently greater EAR in active youth populations may just represent the suggested general insufficiency of current recommendations for children (12). Therefore, to specifically address the impact of exercise on dietary protein requirements, additional studies including both nonexercise and exercising youth and rest and exercise days within a given study and utilizing identical methodology (e.g., NBAL or IAAO) are required to confirm or refute the apparent exercise-induced increase in daily requirements.
Comparison of exercise-induced increase in EAR for adults (i.e., ~1.7-fold) seems to reveal relatively greater protein requirement compared with active children and adolescents (i.e., ~1.4 and ~1.5-fold, respectively; Fig. 1). In our hands, children and adolescents performing a simulated soccer match (i.e., the Loughborough Intermittent Shuttle Test) have EARs for protein that are either similar to or only up to ~1.2-fold greater (Volterman KA, Brooks JC, Rocha AC, Malowany J, Gillen JB, West DW, Courtney-Martin G, Pencharz PB, Moore DR. Unpublished data, 2018.) than their sedentary peers (12) compared with the ~1.3–1.5-fold greater EAR for adults performing an identical exercise task (11,24,25). Collectively, these data suggest that although active children and adolescents may have similar daily requirements as active adults (i.e., ~1.4–1.6 g·kg−1·d−1) due to the increased need for dietary amino acids to support growth, active youth ultimately may be relatively more “anabolically sensitive” to dietary protein than similarly active adults. Alternatively, the greater protein requirement in adults performing aerobic-based exercise has been suggested to reflect the need to replace exercise-induced amino acid oxidative losses (22,26). However, at similar relative exercise intensities, children have been reported to have a greater reliance on fat as a source of fuel than adults (27). Although we currently do not know the metabolic capacity for amino acid oxidation during exercise in children or adolescents, metabolic alterations such as training-induced increases aerobic capacity and the presence of estrogen that translate into greater reliance on fat compared with carbohydrate as a fuel in adults also are associated with reductions in amino acid oxidation (28). Thus, the relatively attenuated increase in protein requirements in active youth may reflect an immaturity in amino acid oxidative capacity compared with adults. Ultimately, additional research is warranted in active children to confirm whether these trends for a greater EAR are justified and, if so, to elucidate the physiological basis for these increased requirements relative to their maturational stage. Nevertheless, active children and adolescents consuming adequate energy and ~1.6 g·kg−1·d−1 of dietary protein likely would meet the metabolic demand for this important nutrient to support their growth and development.
ASSESSMENT OF PROTEIN METABOLISM IN YOUTH
Body proteins are continually synthesized from free amino acids and broken down into their constituent amino acids in a process called protein turnover. This turnover functions to remodel body proteins and, when synthesis exceeds breakdown, support lean mass growth through the induction of a net positive protein balance. Protein turnover at the whole-body level can be measured through stable isotope methodologies (e.g., oral [15N]glycine ingestion or intravenous [13C]leucine infusion) that generally are regarded as safe and can be used in a variety of populations including children. Studies in adults have shown that the increase in protein synthesis and net protein balance (i.e., net anabolism) with exercise and nutrition is often of greater relative magnitude when measured at the muscle compared with the whole-body level (29). The argument, therefore, could be put forth that because children are growing all lean body tissues simultaneously, it is relatively more important to measure protein metabolism and protein balance at the whole-body level with the corollary that these would, to a certain degree, be mirrored by changes in the muscle as well. Thus, the following sections will summarize recent developments in the study of protein turnover in youth from whole-body stable isotope methodologies. However, future studies in children and adolescents may benefit from the emergence of minimally invasive oral tracer methodologies (i.e., 2H2O) that may provide surrogate measures of muscle protein metabolism from the synthesis of muscle-specific proteins (e.g., muscle creatine kinase) from blood samples (30).
EXERCISE-INDUCED CHANGES IN PROTEIN METABOLISM
The remodeling and growth of lean tissue ultimately are underpinned by changes in protein turnover. Whereas targeted exercise programs may (31,32) or may not (33) increase muscle and lean body mass in children and adolescents, there is substantial evidence that an active lifestyle incorporating high levels of moderate-to-vigorous physical activity is associated with greater total body lean mass (2–4). Thus, resistance-trained adults who are increasing muscle mass (i.e., “growing”) could be the only adult-surrogate to active youth who are concurrently growing. It has been shown that increasing physical activity in children is associated with a reduction in whole-body protein turnover (34,35). Although this may seem counterintuitive, the greater nitrogen retention associated with this exercise-induced reduction in nitrogen flux was suggested to represent a repartitioning of amino acids to growing tissues (e.g., muscle) that have lower turnover rates (34,35).
Although this hypothesis is difficult to assess in the acute setting without the direct sampling of skeletal muscle, which is not ethically feasible in healthy children, this concept does have some support in adults. For example, whole-body protein metabolism has been shown to be reduced in adults in response to a period of chronic resistance training despite this representing a period in which skeletal muscle protein turnover is increased and muscle hypertrophy and lean mass gains have occurred (36,37). In fact, oral [15N]glycine-determined rates of whole-body nitrogen flux, although potentially greater in children before training (Fig. 2A), similarly are reduced ~0.6-fold in children after 6 wk of resistance training as in adults after 12 wk of training (Fig. 2B), both situations in which lean mass accrual had occurred (~0.53 and ~0.34% per wk, respectively) (35,36). Furthermore, 24-h nitrogen retention, although greater in children before training (Fig. 2A), similarly is increased ~2.2-fold after training in children and adults in these same studies (35,36) (Fig. 2B).
Collectively, these data suggest that children experience directionally similar changes in free-living rates of whole-body protein metabolism in response to the anabolic effects of exercise. However, the greater relative NBAL suggests that children have a greater anabolic sensitivity (i.e., greater net balance at a suboptimal protein intake) or anabolic capacity (i.e., greater net balance at a similar protein intake) compared with adults.
DIETARY PROTEIN TO ENHANCE EXERCISE-INDUCED PROTEIN METABOLISM
Recent research in children has shown that postexercise protein ingestion enhances whole-body anabolism in active children (15,38), which is similar to studies in adults (29). We recently conducted the first ingested protein dose-response study in active children utilizing the criterion standard primed constant [13C]leucine infusion and demonstrated that, similar to adults (39), children display a dose-dependent increase in whole-body net leucine balance up to 15 g (i.e., ~0.33 g·kg−1) of milk protein ingestion after exercise (40). In addition, both children and adults show evidence of an acute nutrient overload in response to dietary protein ingestion, as suggested by an increase in plasma amino acid concentrations concomitant with a plateau in amino acid oxidation at the highest protein intakes (i.e., >0.33 g·kg−1) (39,40). Interestingly, the congruence between rates of the liver export protein albumin and mixed muscle protein synthesis in adults could suggest most, if not all, of the amino acid-sensitive protein pools within the body similarly were maximized at this moderate protein ingestion (39), in which case the fate of the increased circulating amino acids with greater protein intakes eventually may have be directed toward oxidative catabolism. Given that muscle biopsies are not possible in children, it would be interesting to determine whether plasma albumin synthesis similarly plateaus in active children in response to dietary protein ingestion, which ultimately may provide a proxy for a maximal muscle protein synthetic response in this population. Nevertheless, single-meal protein intakes greater than ~0.25–0.3 g·kg−1 in adults and children may not be the most efficient means to ingest dietary protein if the goal is to maximize muscle (39,41) and whole-body anabolism (40) while minimizing oxidative catabolism.
To determine the relative anabolic sensitivity of different populations after exercise, it is more useful to assess the response to a suboptimal dietary protein intake (i.e., less than ~0.25 g·kg−1) and under similar metabolic conditions. Levenhagen et al. (29) determined whole-body net balance via a primed [13C]leucine infusion in adults over 3 h of recovery after an hour of cycling (~70% V˙O2peak) in response to the ingestion of a protein-free mixed macronutrient beverage and one containing 10 g of milk protein (~0.13 g·kg−1). This compares reasonably well with our recent study in children that used 3 × 20 min of variable intensity cycling before ingesting isoenergetic protein-free or milk-protein (i.e., 5 g or ~0.11 g·kg−1) carbohydrate beverages (40). Compared with similarly exercised adults, whole-body net leucine balance was less negative after exercise in children when consuming a protein-free beverage (Fig. 3). In addition, despite a similar increase in essential amino acid concentration in children (~1.25-fold) (40) and adults (~1.33-fold) (29) after consuming a moderate protein intake (i.e., ~0.11–0.13 g·kg−1), the increase in net leucine balance was greater in children than adults (Fig. 3). In addition, the positive net leucine balance we observed with the ingestion of ~0.11 g protein·kg−1 (~0.037 g protein·kg−1·h−1) after exercise in active children (40) is in contrast to the neutral leucine balance with the ingestion of ~0.04 g protein·kg−1·h−1 in nonexercising children (42), suggesting that similar to adults (43) exercise may sensitize children to the anabolic effects of dietary amino acids. Thus, although no studies directly have compared the relative anabolic sensitivity with dietary amino acids after a bolus protein ingestion between active and inactive pediatric populations and between active youth and adult populations, the apparently greater whole-body anabolism reported in our recent study (40) in response to low protein intakes could suggest that children are relatively more anabolically sensitive to dietary protein than their nonexercising peers as well as active adults as a means to support their lean mass growth and development.
Protein Intake Timing and Pattern
Western diets typically are characterized by an unequal dietary protein distribution and feature the majority of the daily intake during the evening meal (44). It has been demonstrated recently that a balanced protein intake is associated with greater daily rates of muscle protein synthesis at rest in adults compared with an unbalanced intake (45). Given the diurnal variation of muscle and whole-body protein metabolism and the requirement for postprandial protein gains to offset overnight and fasted protein losses, the greater anabolism with a balanced distribution may be related to a more efficient stimulation of muscle and whole-body protein synthesis during the morning postprandial period.
We recently sought to determine if breakfast protein intake influenced the ability to offset the fasted, overnight catabolism and sustain a greater acute whole-body anabolism in children (46). Similar to adults (47) and previous reports in children (34,35), we observed that children were in a negative protein balance during the overnight period (46), which highlights the importance of effectively replacing these transient overnight losses during the waking period to induce a positive 24-h balance to support growth. Consistent with the anabolic effects of protein, breakfast protein intakes ranging from 0 to 21 g (i.e., up to ~0.7 g·kg−1) resulted in a dose-dependent increase in whole-body net protein balance during a 9-h simulated school day that was mediated primarily by the stimulation of whole-body protein synthesis. Thus, breakfast protein intake would seem to be an important mediator of the daytime postprandial anabolism. However, following these same children for an entire 24-h period, we observed that whole-body net protein balance was similarly positive when consuming iso-protein diets (46), suggesting the daily pattern of protein intake may be less important for overall net growth in children provided a sufficient daily intake is met.
These data are somewhat at odds with previous work in children demonstrating that a redistribution of animal protein from the evening to the morning, which subsequently resulted in a more balanced daily protein intake, resulted in a greater net nitrogen retention at relatively high (i.e., ~2 g·kg−1·d−1) protein intakes (48). Thus, additional research is warranted to determine to what extent the distribution of dietary protein intake, independent of the total intake, may have on protein metabolism and, ultimately, lean mass growth in healthy active children.
Whereas children and adolescents consistently gain lean mass, parallels with otherwise weight-stable adults may be most relevant in populations performing resistance exercise. In this respect, resistance exercise in adults may somewhat recapitulate the anabolic environment of youth as it is fundamentally anabolic in nature and increases the sensitivity of skeletal muscle toward dietary amino acids for up to 24 h (43). We also have demonstrated that the ingestion of four moderate (i.e., ~0.25 g·kg−1) protein intakes every 3 h after resistance supports greater rates of myofibrillar protein synthesis (49) and whole-body net protein balance (50) over 12 h of recovery. These data highlight that the pattern of protein intake during a prolonged recovery period is important to support protein remodeling and muscle protein synthesis. Based on these results, adults consuming five meals ~0.25–0.3 g·kg−1) of protein within a ~16-h wake cycle would provide an optimal delivery of amino acid to skeletal muscle that would support maximal rates of muscle protein synthesis and, overtime, potentially support greater lean mass growth. To test whether the pattern of protein intake similarly may affect acute anabolism (i.e., net protein balance) in active growing children, we extended our acute protein dose-response study (40) by providing the same children with a reciprocal protein intake at 3 h of recovery and monitoring their 24-h whole-body net protein balance via oral [15N]glycine ingestion (51). In this way, all participants received an identical 15 g of milk protein (~0.33 g·kg−1) over 3 h of recovery with the exception that the pattern was split into single (0/15 g or 15/0 g at 0 and 3 h, respectively) or multiple (5/10 g or 10/5 g at 0 and 3 h, respectively) protein doses. We observed that despite a clear ingested protein dose-response during the acute exercise and 3-h recovery period, 24-h whole-body net protein balance was greater with the multiple smaller protein intakes compared with a single bolus of 15 g (i.e., ~0.33 g·kg−1) consumed either immediately or at 3 h of recovery (51). Thus, similar to adults during recovery from resistance exercise (49), our data suggest that multiple smaller protein meals containing ~0.11–0.21 g·kg−1 support a greater acute anabolism during recovery from physical activity in children consuming a moderate (i.e., 1.2 g·kg−1·d−1) protein diet (51).
From the limited research available, it seems that children display similar exercise-induced changes in whole-body protein metabolism as adults (Fig. 2), which would be consistent with the ability of physical activity to remodel lean (and especially muscle) tissue. Moreover, similar to adults, dietary protein ingestion increases postexercise net protein balance. However, it is unclear if this greater net protein balance, which could be interpreted as an acute surrogate marker of “growth,” is summative to the normal lean mass gains that occur in active children such that overall lean mass growth is augmented over time with optimized dietary protein ingestion. Alternatively, active youth athletes also may be interested in enhancing the recovery from and adaptation to exercise, which could include enhancing strength, power, or fatigue resistance. Although there is some support for protein supplementation per se to enhance some facets of postexercise recovery or performance in adults (e.g., (52)), we currently lack performance-based and longer-term intervention studies in active youth to conclude whether dietary protein ingestion, either as supplements or within a whole food diet, influences exercise performance in active pediatric populations.
Consistent with the need for dietary amino acids to support growth, active children seem to be relatively more anabolically sensitive to these important nutrients than similarly active young adults. Extending this comparison across the lifespan, it is generally observed that older adults require a greater protein intake to maximize muscle protein synthesis at rest (41) and after exercise (53), which is consistent with an insipid age-related anabolic resistance. Thus, during periods of rapid lean mass growth such as in active youth, and especially adolescents (42), there is a greater ability to use dietary amino acids for increasing net protein balance that wanes with age and ultimately translates into the characteristic loss of lean mass in older adulthood (Fig. 4).
Importantly, anabolic resistance to dietary protein can manifest ostensibly at any age in response to a reduction in physical activity, either with overt disuse such as casting and bedrest (as reviewed by (54)) or more “benign” forms such as low daily step counts (55). Moreover, comorbidities of an inactive lifestyle such as excess body fat also may independently impair the nutrient-induced stimulation of muscle protein synthesis in adults (56). The regrettable reality of today’s youth is that a vast majority do not meet minimum physical activity guidelines (57) and, relatedly, up to ~35% may be classified as overweight or obese (58). Given that inactive children have less lean mass than their physical active peers (2–4), there is an urgent need to determine the impact of a sedentary lifestyle (with and without excess body fat) in childhood and adolescence on the ability to use dietary amino acids to remodel (and ultimately build) lean mass. It is possible that similar to inactive adults, sedentary children also may display a relative anabolic resistance to dietary amino acids that ultimately constrains their ability to develop a high quantity and quality of lean mass that normally is found in active youth.
Therefore, future studies, utilizing traditional whole-body tracers and newer minimally invasive surrogate muscle protein synthetic methods (30), need to better characterize the impact of inactivity and the restoration of activity on protein metabolism in youth to advance our understanding of the negative impact of physical inactivity on lean mass growth and development. The knowledge ultimately could extend the discussion on the deleterious effects of inactivity beyond the traditional pediatric scope of aerobic fitness, metabolic health, and body fatness and toward the negative impact it may impart on the optimal growth and development of lean mass.
Consistent with the anabolic effects of physical activity, whole-body protein balance is enhanced in active children relative to their inactive peers and similarly active adults. Evidence suggests that, similar to athletic adult populations (13), daily protein requirements in active children and adolescents may be elevated by up to ~60% above current estimates with daily intakes of ~1.6 g·kg−1·d−1 likely meeting the metabolic demand for this important macronutrient. Active youth also obtain similar benefits to whole-body protein metabolism as adults from the ingestion of dietary amino acids, which includes an enhancement in whole-body net protein balance with protein ingestion immediately and at regular intervals after exercise. Although meal protein intakes of ~0.25 g·kg−1 likely would maximize whole-body net protein balance and minimize irreversible amino acid oxidation, consistent with the need to support normal somatic growth that is augmented by a physically active lifestyle, active youth seem to have a greater net protein balance than similarly active adults at suboptimal (i.e., greater anabolic sensitivity) and optimal (i.e., greater anabolic capacity) dietary protein intakes. Thus, with respect to exercise-induced changes in protein metabolism and the ability to assimilate dietary protein into a positive net protein balance (i.e., anabolism), active children and adolescents are not exactly “little adults” but arguably “better” versions of their older selves.
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