Introduction
The prevalence of obesity is growing worldwide [
1]. This disease is a significant public health issue [
2] as it favors the development of several other comorbidities such as diabetes [
3], cardiovascular disease [
4], and several types of cancer [
5] compromising quality of life and mortality risk. Obesity is particularly concerning during childhood and adolescence because these developmental phases are pivotal for the acquisition of healthy lifestyle habits [
6] and due to the associated consequences of the early instalment of overweight and obesity for adult cardiometabolic disease risk [
7••]. In this context, severe cases of childhood and adolescent obesity are particularly worrisome [
8].
Bariatric surgery (BS) is a well-established treatment for obesity [
9,
10] and many of its related comorbidities. This evidence is well documented in adults [
11] and also, increasingly, in adolescents [
12,
13]. However, the greater reduction in body weight promoted by BS is also tied to substantial changes in other body composition components [
14] such as significant decreases in muscle [
15•] and bone [
16,
17•] mass. Consequently, when performed in adolescents, BS-induced lean mass losses raise some concerns due to their possible negative influence during the growth and development phase [
18,
19••]. The energy deprivation and accelerated weight loss in the first months post-BS, as well as the risk of nutritional deficiencies [
20], which are more prevalent after malabsorptive procedures such as the Roux-en-Y gastric bypass (RYGB) and which are aggravated by the low adherence of adolescents to nutritional supplementation recommendations [
21] could have detrimental metabolic and musculoskeletal consequences, especially during adolescents growth [
22]. Despite these concerns, and also considering the new expanded definition of adolescence, which goes now from 10 to 24 years of age [
23], available follow-up data in children and adolescents who underwent BS suggest a normal growth at 2 [
24] and 5 years [
25] after sleeve gastrectomy (SG). Nevertheless, the long-term potential consequences of BS in pediatric ages remain controversial and might differ substantially according to the specific population analyzed [
26] and bariatric procedure employed [
27].
Despite the increasing adoption of bariatric procedures for adolescents with severe obesity, only few studies with a small number of subjects have assessed changes in body composition in this population. In addition, there is a lack of systematic reviews with meta-analysis analyzing the available data on the effects of BS on adolescent’s body composition. Consequently, the aim of this systematic review with meta-analysis is to characterize the short- and long-term effects of BS on body composition of children, adolescents, and young adults and to determine how these changes are influenced by different bariatric procedures.
Discussion
The effect of BS in adults body composition is widely documented, but few studies have assessed these outcomes in children and adolescents. There is some concern of performing this procedure during growth due to the potentially extensive lean and fat-free mass losses, which may have future negative health consequences. Our analysis suggests that BS, similarly to adults, is extremely effective in reducing fat mass, body weight, BMI, and waist circumference in adolescents assessed 12 months after surgery. Despite these benefits, a significant reduction in lean mass and fat-free mass was also observed. Body weight, BMI, and fat mass losses seem to be higher in boys than in girls. Both types of surgery, RYGB and SG, were effective in reducing body fat and obesity related anthropometric outcomes; however, higher losses seem to be observed in patients who underwent RYGB. Finally, in patients submitted to RYGB, body composition reductions were more pronounced in the first-year post-surgery whereas in the second year a stabilization was frequently observed.
Several studies have investigated the effect of BS on body weight and BMI in a younger population. However, few studies have assessed changes in body composition in this population. Beyond the positive reductions observed in body weight, fat mass, BMI, and waist circumference, a reduction of obesity-related comorbidities after surgery is also documented [
24], evidencing BS effectiveness during adolescence and young adulthood for improving cardiometabolic health. Despite these benefits, the surgery associated energy deprivation also leads to significant decreases in muscle mass. This might negatively affect whole-body metabolism such as aerobic capacity [
62], regulation of resting metabolic rate, and possible lead to long-term musculoskeletal issues [
63]. Of note, muscle mass losses in adolescents have been associated with an increased risk of metabolic syndrome [
64] and nonalcoholic fatty liver disease development [
65]. Noteworthy, in weight loss multidisciplinary intervention programs (MIP), children and adolescents with obesity were able to, not only decrease their body weight and fat mass, but also maintain [
66‐
68] or even increase their lean mass [
69] and fat-free mass [
70] percentage. In contrast, patients who underwent SG showed a higher muscle mass loss and protein-energy malnutrition than those undergoing MIP [
71]. Therefore, the question remains if the drastic energy deprivation and associated gastrointestinal anatomic, physiologic, and endocrine changes associated with bariatric surgery [
72], and the consequently pronounced body weight loss during the growth period could lead to negative long-term consequences, especially of the musculoskeletal system.
Our results show that whole-body BMD did not decrease 12 months after BS, contrasting with most of the findings in adults [
73]. However, these results must be carefully interpreted, firstly due to the reduced number of studies included in our analysis (only three studies) and secondly, because during adolescence bone mass is expected to increase. Therefore, since adolescents are going through an active bone modeling phase, increases in bone mass should normally be anticipated. Of note, the peak bone mass (PBM), which is considered the highest amount of bone mass accumulated at the end of the growth period, can be reached during the second [
74], or even the third decade of life [
75,
76]. PBM is an important determinant of bone strength and bone health [
77,
78] and the age of higher bone accrual acquisition is approximately 12 years for girls and 14 years for boys [
79]. In this regard, a possible negative effect on bone acquisition promoted by bariatric surgery during this phase, such as due to energy deprivation, might impair PBM achievement and consequently increase the risk of age-related bone disorders, such as osteoporosis, and increased fracture risk [
80]. Of note, it is important to recognize that severe obesity, by itself, is also considered harmful for bone quality [
81]. Therefore, it is possible that performing BS during the period of accelerated growth and development might impair bone health to the same extent as long term exposure to severe obesity. Curiously, one study observed significantly reduced fat-free mass in adolescents 5 years post-RYGB in comparison with non-surgical controls [
60]. Although our results suggested no negative effect of BS on bone mass, the question remains whether the growth observed was sufficient for that expected period of age. As a major limitation hindering the possibility to adequality address this question, few studies provide a control group to compare bone accrual during follow-up after BS. For instance, in Misra et al. 2020b [
32••], the adjusted BMD increased less in the surgical group in comparison with non-surgical controls, and the BMD
Z-score also decreased in most studies [
32••,
38,
40]. In this context, in order to identify bone growth restrictions, we performed a BMD
Z-score analysis 12 months after surgery, but no significant differences were found.
Although few studies reported data according to sex, our results are in agreement with most of the current literature available for adults, in which males present higher reductions in fat mass [
82] and higher preservation of lean mass [
83] when compared to females. Curiously, our study indicates that, in adolescents, despite a higher fat mass loss observed in boys [
38,
39,
60], lean mass [
38] and fat-free mass [
60] tend to be more preserved than in girls. Interestingly, the sensitivity analysis showed that the heterogeneity in lean mass following RYGB decreased after removing the study of Beamish et al. A (only girls) [
38] (Supplementary Table
4; Analysis 11). Moreover, both studies providing data by sex, [
38,
55] reported higher lean mass losses in girls compared to boys (Beamish et al. B) or when results are presented for both sexes together [
60]. This result suggests that RYGB might promote higher lean mass losses in girls than in boys. This higher lean mass preservation in boys might be explained by a favorable hormonal context with higher circulating testosterone levels in boys during adolescence, which might contribute to mitigating the detrimental effect of BS on lean mass [
84]. The higher body weight loss observed in boys can also be related to their higher baseline values, providing a greater margin for weight loss compared to girls. Despite these observations, due to the scarcity of studies providing data according to sex, it was not possible to perform a meta-analysis to clarify if the effect of BS in adolescents’ body composition is sex dependent.
Regarding the analysis according to the type of surgery, both procedures analyzed (SG and RYGB) promoted a reduction in all the selected body composition and anthropometric outcomes in adolescents, except for bone mass. Regarding the results heterogeneity, when data was analyzed according to type of surgery and the study of Dubnov-Raz et al. [
39] was removed, a heterogeneity of 0% was achieved. This suggests that different surgical procedures may have different effects on body composition outcomes, increasing the heterogeneity in our analysis. In fact, different types of surgery can lead to different long-term effects [
46]. Of note, a recent meta-analysis carried out in data from adults showed that, although RYGB promoted higher lean mass losses than LAGB, changes following RYGB and SG were similar [
85]. Notwithstanding, it is important to consider that, as a malabsorptive surgery, RYGB could elicit more pronounced negative consequences to the musculoskeletal system [
86]. In the present analysis, despite patients who underwent RYGB presenting higher losses for all body composition and anthropometric outcomes, it was not possible to directly compare the two types of surgical procedures (SG and RYGB) and determine which was the most effective. It is also important to consider that differences in patient’s baseline characteristics might have influenced the results heterogeneity.
Finally, to assess the long-term effect of BS, we compared the mean differences between the first and second year after RYGB. As expected, and similarly to what is observed in adults, body weight, BMI, lean, and fat mass decreased significantly during the first post-surgery year [
15•]. Some studies have observed that, after 12 months, fat mass continues to decrease, whereas lean mass could be maintained or even increase [
56,
59]. Our meta-analysis, however, shows only the preservation of these outcomes in a period beyond 12 months. Only one study achieved a significant decrease in fat mass and fat-free mass after the first 12 months following surgery, which could be related to the higher dropout observed in this study [
13]. The only study with a follow-up of 5 years after RYGB found no significant regain in body weight or fat mass [
60]. Despite no fat-free mass regains being observed 5 years post-surgery, protein supplementation preserved fat-free mass better than in patients who did not follow this nutritional recommendation (− 6.5 ± 4.4 kg versus − 10.5 ± 5.4;
p = 0.01). This highlights the need to better understand the long-term implication of BS on body composition and to develop adequate countermeasures, such as physical exercise programs and nutritional supplementation, to tackle possible future negative effects.
The high heterogeneity in our overall analysis, possibly caused by the type of surgery or sex-related differences in the response to BS, led to some inconsistencies in our results which rated the changes in body composition outcomes with a “low certainty of evidence” status. For an accurate analysis to determine the effect of different types of surgery or how body composition outcomes may vary according to sex, future studies should provide separate data by sex and surgical procedure.
The major strength of our review is to be the first one to summarize the available evidence on the effect of BS on adolescents’ body composition and to characterize these changes according to type of surgical procedure and adolescent’s sex. As a major limitation, we identified only a reduced number of studies assessing body composition changes in adolescents and no studies assessing these outcomes in children. Moreover, some reports included in our analysis were derived from the same study and analyzed the same sample, which may have contributed to bias our results.
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