Approximately 20% of adolescents in the United States are obese (1), and without an effective intervention, as many as 80% will become obese adults (2). The most successful adolescent weight management programs offer a combination of diet, exercise, and behavioral counseling (3, 4); however, it is often difficult to determine which practices within each program component elicit the most beneficial effects on weight loss outcomes (5, 6). Independent of how it is achieved, weight loss is a result of energy expenditure exceeding energy intake. Given the inability to discern whether diet or physical inactivity is the stronger contributor to pediatric obesity (7), both energy intake and expenditure must be considered when developing weight loss prevention and intervention programs for adolescents.
Approximately 70% of total daily energy expenditure is attributed to resting energy expenditure (REE), and fat-free mass (FFM) is the largest contributor to REE during both adolescence and adulthood (8). Considering the strong influence of FFM on energy balance, the preservation of FFM following participation in adolescent weight management programs is generally recognized as having a positive impact on long-term outcomes (9, 10). It follows that FFM-sparing strategies (e.g., increased protein intake and resistance training) are often implemented into adolescent weight management programs (11–13). However, over 25% of the excess weight in obese adolescents is attributed to elevations in FFM (14). Therefore, if the common, yet conflicting, goals of retaining or increasing FFM while subsequently maximizing weight loss (15, 16) are to be realized, weight management strategies may need to emphasize one goal over the other.
In previous studies reporting increased FFM following participation in an adolescent weight management program, body weight was either unchanged or increased (16–18). Considering the substantial contribution of FFM to excess body weight in obese adolescents, a further understanding of the relationship between FFM and REE may provide insight as to whether total weight reduction or the preservation of FFM exerts the greater influence on long-term weight loss outcomes. Additionally, while REE is positively related to both body weight and FFM, the REE-to-FFM ratio (REE-to-FFM) is dependent upon the composition of FFM (i.e., organ tissue, skeletal muscle, fluid, and bone) (19, 20). Given that the proportion of each component varies between adolescents and adults and lean and obese individuals (10, 19, 21), the influence of FFM on long-term energy balance with respect to the treatment of adolescent obesity deserves further exploration. Last, examining the physiologic basis behind fundamental weight loss strategies and the supporting evidence for their inclusion in pediatric weight management programs may provide further awareness and improve current treatment efforts (22). Therefore, the purpose of this review is to 1) describe the influence of FFM on REE, 2) summarize the existing evidence regarding the efficacy of FFM-sparing treatment strategies in obese adolescents, and 3) examine the interrelationships between changes in FFM, REE, and body weight during negative energy balance.
Fat-free mass and resting energy expenditure
Fat-free mass composition and REE-to-FFM
Resting energy expenditure is a measure of the body’s total basal cellular activity. Therefore, REE-to-FFM is a function of the volume of energetic cells, or the body cell mass, relative to the FFM compartment (23). The volume of body cell mass in relation to FFM during adolescence differs with respect to age, body weight, and gender (24, 25) due to differences in water, protein, glycogen, and mineral content (19, 26). Finally, the mass of each of these FFM constituents must also be considered with respect to their distribution across the body tissues, as both the contribution of organ mass to FFM and the energy expenditure of the individual organs appears to be greater in adolescents than adults (19, 24).
During adolescence, FFM is comprised of 42% skeletal muscle and 8% organ tissue, with the remainder attributed to bone and extracellular fluid (19, 20). Liver, heart, kidney, brain (∼450 kcal·kg–1·day–1), and skeletal muscle (∼15 kcal·kg–1·day–1) tissue account for nearly all of the REE, while bone and extracellular fluid and matrix contribute <1 kcal·kg–1·day–1 (19, 20). Of note, obese youth have a 1.8% greater hydration of FFM compared to their lean counterparts (14), suggestive of a relatively smaller contribution of more metabolically active tissues to FFM, thereby, decreasing REE-to-FFM. However, due to current limitations in the assessment of body composition (discussed below in the Methodological considerations section) and differences in methodologies used across studies, it is unclear whether REE-to-FFM is decreased in obese relative to lean adolescents (21, 27–29). In contrast, the considerably greater resting energy requirement of organ relative to skeletal muscle tissue (20) indicates that an increase in the skeletal muscle-to-organ mass ratio, as occurs during both the transition from adolescence into adulthood and in obesity, would coincide with a decreased REE-to-FFM (19). Not only REE-to-FFM but also REE in relation to the total body weight is higher in adolescents than adults (24), suggesting that maintenance of obesity-related elevations in FFM along with a reduction in the energy expenditure attributed to FFM during young adulthood would be energetically disadvantageous to long-term weight control.
Since REE-to-FFM is a function of the composition of FFM and the composition of FFM influences the accuracies of the various body composition measurement techniques (14, 30, 31), consideration must also be given to the body composition assessment method used when evaluating the relationship between REE and FFM. The preferred method for estimating body composition in youth is the combination of measures of fat, water, protein, and mineral content to yield a four-component model (32). However, due to technical and cost limitations associated with this method, body composition is most often assessed using more practical, but less accurate, two-compartment models that divide the body into FFM and fat mass. Whereas the calculation of FFM from total body water and dual energy X-ray absorptiometry (DXA) assumes a constant hydration of FFM, greater hydration levels in obese adolescents could influence the accuracy of these methods. For instance, DXA was found to overestimate the loss of fat mass and gains in skeletal muscle in obese adolescents when compared to magnetic resonance imaging (31). On the other hand, bioelectrical impedance analysis may be more sensitive to differences in FFM hydration between obese and normal weight youth (30), although this method generally provides less accurate estimates of body composition than both DXA and air displacement plethysmography (33). Last, the composition of exercise-spared FFM during/following weight loss is not well defined (34) and deserves further evaluation when considering the variability in exercise programming across adolescent weight management programs.
FFM-sparing treatment strategies
High-protein diets and resistance training
Owing to the strong contribution of FFM to REE, dietary and exercise strategies known to preserve or even increase FFM are often implemented into adolescent weight management programs (12, 13, 35–37). Even during severe caloric restriction (≤800 kcal·day–1), increased protein consumption has been shown to preserve both the amount and composition of FFM in obese adolescents (11, 35). Whereas exercise is known to attenuate the loss of FFM during negative energy balance, this effect is more pronounced following resistance compared to aerobic training. However, when considering the inverse relationship between FFM and REE-to-FFM and the reduction in REE-to-FFM from adolescence into adulthood (19), the weight loss and health outcomes associated with increased protein consumption and resistance training may be of greater significance than their respective effects on FFM. In accordance, the magnitude of reduction in body weight (i.e., the degree of negative energy balance) rather than the proportion of calories coming from protein intake or the relative retention of FFM appears to be the strongest determinant of the change in REE-to-FFM in obese adolescents (10, 11, 35).
Considerations for growth and development
In contrast to the treatment of adult obesity, the impact of weight loss on growth and development is of concern in the pediatric population. During adolescence, growth contributes to approximately 7% of REE-to-FFM (25) or 2%–4% of the total energy requirements (38). Importantly, growth appears to continue unimpeded in obese adolescents consuming as few as 500 kcal·kg–1·day–1 (35, 39, 40), perhaps due to the earlier onset of puberty in obese compared to lean youth (41, 42). Additionally, the degree of reduction in FFM during weight loss is inversely related to the initial body fatness (43, 44). This inherent preferential loss of fat mass further alleviates concerns regarding the loss of FFM in obese adolescents. In turn, the risk of sarcopenic obesity also appears to be of minimal concern in adolescents, as the ratio of skeletal muscle to adipose tissue is highest during youth and young adulthood (45). Although body weight may normalize following moderate weight loss or by simply attenuating weight gain in younger youth (46), the observation that many obese adolescents will benefit only from substantial weight loss (47) further supports the utilization of strategies to maximize weight loss taking precedence over those to retain FFM.
Efficacy of high-protein diets and resistance training in obese adolescents
Since developmental gains in FFM appear to be unaffected by obesity treatment during adolescence, FFM-sparing program components on long-term weight loss outcomes may be more efficacious in adults than adolescents. Whereas an increase in dietary protein content has been shown to attenuate weight regain in adults (48), both short- and long-term weight loss outcomes were similar among obese adolescents consuming diets comprised of between 15% and 30% protein (12, 36, 49). These findings may be partly explained by the lack of difference in hunger control observed between adolescents following either high- or low-protein diets (49, 50). Similarly, the lack of evidence supporting the efficacy of resistance training in the treatment of adolescent obesity (13, 16) may be explained by the greater caloric expenditure required for the performance of aerobic as opposed to resistance training (51). In accordance, the former is generally associated with slightly greater improvements in body weight and composition in obese adolescents, despite greater gains in skeletal muscle following resistance training (31, 52, 53), perhaps due to a resultant reduction in REE-to-FFM. Taken together, further evaluation of the effects of high-protein diets and resistance training on long-term weight loss outcomes is needed to determine which dietary and exercise practices are most efficacious in the treatment of adolescent obesity.
Fat-free mass and weight loss outcomes
FFM, REE-to-FFM, and weight loss
Given the inability to clearly link FFM-sparing treatment strategies to improved weight loss outcomes in obese adolescents, a better understanding of the influence of FFM on energy balance during weight loss is needed. Considering the five-fold greater contribution of FFM (∼18 kcal·kg–1·day–1) than fat mass (∼3.5 kcal·kg–1·day–1) to REE (54, 55), the preservation of FFM during weight loss is generally believed to elicit the most beneficial effect on energy balance. However, 75% of the FFM lost during energy deficit is attributed to reductions in less metabolically active components (e.g., skeletal muscle, fluid, extracellular matrix) (55–57), while protein catabolism accounts for only 5% of the total weight loss initially and 2.5% over the next several months (34, 56). Such findings may explain the aforementioned lack of difference between high- and low-protein intakes on weight loss outcomes in obese adolescents, as even during long-term fasting, only 25% of the reduction in FFM is due to the loss of protein (57). Therefore, reported reductions in REE-to-FFM in adolescents who successfully preserved FFM during weight loss (10) may be attributed to hormonal changes (58) and/or the loss of fat mass, which, as previously mentioned, is not metabolically inert but can be a significant contributor to REE in obese individuals (59).
As the majority of REE is attributed to organ metabolism, REE-to-FFM decreases with increasing FFM due to a reduction in the relative contribution of organ mass to FFM. In other words, disproportionate increases in less metabolically active FFM components (e.g., bone, fluid, and skeletal muscle) relative to the more active organ tissue may not exert as beneficial of an effect on energy balance as is often perceived and could explain the lack of evidence supporting the use of resistance training in the treatment of adolescent obesity (13). From this, simultaneous reductions in both body fatness and FFM may not be detrimental to long-term energy balance, particularly when considering the excess FFM in obese adolescents (14). Furthermore, when considering the generally modest reductions in body weight following participation in most adolescent weight management programs, the relatively minor loss of more metabolically active tissues during weight loss suggest that absolute weight loss should be encouraged over the retention of FFM.
FFM and weight maintenance
The relationship between the change in FFM during weight loss and long-term weight regulation in obese adolescents is relatively unexplored. Schwingshandl et al. (9) reported a beneficial effect of FFM sparing on weight regain after 1 year in a mixed group of 20 obese children and adolescents. In that study, not all participants received the same intervention, and body composition and weight changes were inconsistent. Further evidence of an inverse relationship between the change in FFM following weight loss and subsequent weight regain in adolescents is needed, as increased FFM may lead to augmented hunger signaling (60), potentially exacerbated by reductions in the satiety hormone leptin following weight loss (61). While reductions in energy intake have been observed over the short-term in obese adolescents who gained FFM during treatment (18, 60), the preservation of and/or increases in FFM could bear a negative effect on future dietary habits, as FFM is the strongest predictor of energy intake in adult males (62). Alternatively, maintenance of body composition at a lower absolute FFM would require less energy intake (63) and result in an increased REE-to-FFM (19).
While fat loss is certainly preferential to reductions in FFM, retention of FFM without reductions in weight or body fatness may not always be energetically advantageous to long-term outcomes. The influence of FFM on energy balance is mediated by REE-to-FFM, and REE-to-FFM is inversely proportional to FFM. Considering the strong dependency of REE on not only FFM but also total body weight in obese adolescents, whether long-term energy balance is more strongly influenced by weight loss-induced reductions in REE and REE-to-FFM or the increased REE relative to total body weight (10) requires further exploration. Regardless of whether REE, REE-to-FFM, or REE-to-body weight is the strongest determinant of energy balance, it seems that simultaneous maximization of each would have the most desirable effect on long-term weight loss outcomes (55).
MGB and RKE prepared the manuscript and critically reviewed the submission. Both authors read and approved the final manuscript. The authors declare that they have no competing interests. No funding was received for the drafting of this manuscript.
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About the article
Published Online: 2014-12-03
Published in Print: 2015-08-01