Full Length ArticleBone outcomes following sleeve gastrectomy in adolescents and young adults with obesity versus non-surgical controls
Introduction
Metabolic and bariatric surgery is an increasingly common treatment strategy in adolescents and young adults with moderate to severe obesity [[1], [2], [3], [4]]. Whereas such surgery is typically associated with a significant improvement in various metabolic parameters, metabolic and bariatric surgery has been associated with deleterious effects on bone health. Several studies in adults indicate that gastric bypass leads to reductions in areal and volumetric bone mineral density (BMD), with negative effects on bone geometry and microarchitecture [[5], [6], [7], [8], [9], [10]]. Similarly, adults undergoing sleeve gastrectomy have a reduction in total hip and femoral neck areal BMD over time [6,[11], [12], [13]]. Some [6,8], though not all [12,13] studies in adults report lesser reductions in total hip and femoral neck BMD following sleeve gastrectomy vs. gastric bypass. A meta-analysis comparing sleeve gastrectomy to bypass reported no differences between groups in post-operative BMD [13]. Metabolic and bariatric surgery has also been associated with an increase in fracture risk [14,15]. Studies comparing fracture risk following gastric bypass vs. sleeve gastrectomy are conflicting with one reporting increased fracture risk in the bypass group alone [16], and another reporting no differences between groups [17].
Adolescence is a time of marked increases in bone accrual towards attainment of peak bone mass, a key determinant of bone health and fracture risk in later life [18]. Studies in other populations suggest that suboptimal bone accrual during adolescence can lead to suboptimal peak bone mass, and an increased risk of fractures in later life [18]. The utilization of metabolic and bariatric surgery as a therapeutic strategy in adolescents with obesity has markedly increased in recent times [19,20], with a 1.8 fold increase reported between 2012 and 2016 in children's hospitals in the United States. It is thus important to determine how and to what extent such surgery impacts bone accrual and morphology during the critical teenage years. A few studies have assessed bone outcomes in adolescents undergoing gastric bypass [21,22], and report significant reductions in whole body bone mineral content and BMD Z-scores following bypass over a two-year period. However, data are lacking regarding the effects of sleeve gastrectomy on bone outcomes in adolescents, particularly data regarding bone structure and strength estimates. Based on some studies in adults, effects may be less severe following sleeve gastrectomy than gastric bypass [6,8] given that certain factors that drive bone loss (such as malabsorption and hormonal changes) are more pronounced following bypass than sleeve procedures. Conversely, given that sleeve gastrectomy in adolescents results in similar reductions in BMI as gastric bypass [23], effects may be comparable for effects primarily related to skeletal unloading following surgery. It is critical to study the impact of sleeve gastrectomy on bone in youth, given that 1) sleeve gastrectomy is now the most commonly performed bariatric procedure in adolescents, 2) because the massive weight loss associated with surgery may affect load related bone physiology, and 3) the effects of surgery on energy metabolism and nutrition may impact bone and metabolic health in youth differently from adults [3].
In order to address this knowledge gap, we examined bone outcomes in youth aged 14–22 years old with moderate-to-severe obesity undergoing sleeve gastrectomy, as well as non-surgical controls of comparable body size matched for age and sex. This age range was chosen given that this is a critical period of peak bone mass acquisition in youth [18]. We hypothesized that as in adults, adolescents undergoing sleeve gastrectomy would have a reduction in areal BMD measures [assessed using dual energy X-ray absorptiometry (DXA)], and that weight loss after sleeve gastrectomy would have a deleterious effect on high resolution peripheral quantitative computed tomography (HRpQCT) measures of bone geometry, microarchitecture and volumetric BMD, associated with reductions in body mass index (BMI) and lean mass.
Section snippets
Participant selection
We enrolled 44 adolescents and young adults aged 14–22 years old with moderate to severe obesity, 22 of whom underwent sleeve gastrectomy (16 female and 6 male) and 22 were non-surgical controls (16 female and 6 male). All participants had a BMI of ≥35 kg/m2 with obesity related complications or a BMI of ≥40 kg/m2 (i.e. met criteria for metabolic and bariatric surgery). Exclusion criteria included (i) current pregnancy or breast feeding (in females), (ii) use of oral glucocorticoids and other
Baseline characteristics
The sleeve gastrectomy (surgical) and non-surgical groups did not differ at baseline for age, weight, BMI z-scores, and percent lean and fat mass, although absolute BMI and fat mass were higher in the surgical vs. non-surgical groups (Table 1). The groups did not differ for baseline levels of 25OHD, calcium, phosphorus and HbA1C. Further, the number of study participants with HbA1C levels in the normal (<5.7%), prediabetes (5.7–6.4%) and diabetes ranges (≥6.5%) did not differ across groups
Discussion
This is the first report of bone outcomes following sleeve gastrectomy in adolescents and young adults, demonstrating the expected reduction in certain DXA measures of aBMD over 12-months in the surgical group. However, we found no differences between groups for changes in total vBMD and strength estimates using HRpQCT and μFEA.
Conclusion
Overall, our study indicates that while there is a reduction in aBMD measures following sleeve gastrectomy in youth, and despite the fact that these youth demonstrate deleterious changes in several HRpQCT parameters at the distal tibia and distal radius over a year, these changes do not appear to reduce strength estimates at skeletal sites at particular risk for fractures over this short duration, likely because of a simultaneous increase in cortical vBMD. Further, reduced body mass may
Grant support
This work was supported by the NIH NIDDK R01 DK103946-01A1 (MM, MAB), NIH K23DK110419-01(VS), P30-DK040561 (VS, FCS), K24DK109940 (MAB), K24 HD071843 (MM), L30 DK118710 (FCS), NIH P30-DK057521 (VS).
CRediT authorship contribution statement
Madhusmita Misra: Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Writing - original draft. Vibha Singhal: Investigation, Supervision, Writing - review & editing. Brian Carmine: Investigation, Writing - review & editing. Amita Bose: Investigation, Writing - review & editing. Megan M. Kelsey: Investigation, Writing - review & editing. Fatima Cody Stanford: Investigation, Supervision, Writing - review & editing. Jennifer Bram: Investigation, Writing -
Declaration of competing interest
The authors have no conflicts of interest to disclose relevant to this paper.
References (53)
- et al.
ASMBS pediatric metabolic and bariatric surgery guidelines, 2018
Surg. Obes. Relat. Dis.
(2018) - et al.
Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue
Bone
(2017) - et al.
Bone loss after bariatric surgery: causes, consequences, and management
Lancet Diabetes Endocrinol.
(2014) - et al.
Changes in bone mineral density and bone metabolism after sleeve gastrectomy: a systematic review and meta-analysis
Surg. Obes. Relat. Dis.
(2019) - et al.
The determinants of peak bone mass
J. Pediatr.
(2017) - et al.
Recent trends of bariatric surgery in adolescent population in the state of New York
Surg. Obes. Relat. Dis.
(2019) - et al.
Trends in volume and utilization outcomes in adolescent metabolic and bariatric surgery at children’s hospitals
J. Adolesc. Health
(2019) - et al.
American Society for Metabolic and Bariatric Surgery Integrated Health Nutritional Guidelines for the surgical weight loss patient 2016 update: micronutrients
Surg. Obes. Relat. Dis.
(2017) - et al.
Large, single-dose, oral vitamin D supplementation in adult populations: a systematic review
Endocr. Pract.
(2014) - et al.
Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography
Bone
(2003)
Quantitative in vivo assessment of bone microarchitecture in the human knee using HR-pQCT
Bone
Suboptimal bone microarchitecure in adolescent girls with obesity compared to normal-weight controls and girls with anorexia nervosa
Bone
The association of overweight and ankle injuries in children
Ambul. Pediatr.
Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy X-ray absorptiometry study
J. Pediatr.
Gastric bypass in obese rats causes bone loss, vitamin D deficiency, metabolic acidosis, and elevated peptide YY
Surg. Obes. Relat. Dis.
Bariatric surgery in adolescents: recent national trends in use and in-hospital outcome
Arch. Pediatr. Adolesc. Med.
National trends in the use of metabolic and bariatric surgery among pediatric patients with severe obesity
JAMA Pediatr.
Pediatric metabolic and bariatric surgery: evidence, barriers, and best practices
Pediatrics
Longitudinal 5-year evaluation of bone density and microarchitecture after Roux-en-Y gastric bypass surgery
J. Clin. Endocrinol. Metab.
Bariatric surgery results in cortical bone loss
J. Clin. Endocrinol. Metab.
Bone structural changes and estimated strength after gastric bypass surgery evaluated by HR-pQCT
Calcif. Tissue Int.
Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: a two-year longitudinal study
Eur. J. Endocrinol.
Effect of bariatric surgery on bone mineral density: comparison of gastric bypass and sleeve gastrectomy
Obes. Surg.
Changes in bone metabolism after sleeve gastrectomy versus gastric bypass: a meta-analysis
Obes. Surg.
Change in fracture risk and fracture pattern after bariatric surgery: nested case-control study
BMJ
Fracture risk after Roux-en-Y gastric bypass vs adjustable gastric banding among Medicare beneficiaries
JAMA Surg.
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