Elsevier

Bone

Volume 134, May 2020, 115290
Bone

Full Length Article
Bone outcomes following sleeve gastrectomy in adolescents and young adults with obesity versus non-surgical controls

https://doi.org/10.1016/j.bone.2020.115290Get rights and content

Highlights

  • Femoral neck and total hip bone mineral density (BMD) (DXA) decreased after surgery

  • % Change in trabecular number was lower in the surgical group at the radius/tibia

  • % Change in trabecular separation was higher in the surgical group at both sites

  • Cortical volumetric BMD increased after surgery at both sites

  • Strength estimates did not change following surgery at either site

Abstract

Background

Sleeve gastrectomy is the most commonly performed weight loss surgery in adolescents with moderate-to-severe obesity. While studies in adults have reported on the deleterious effects of gastric bypass surgery on bone structure and strength estimates, data are lacking for the impact of sleeve gastrectomy on these measures in adolescents.

Objective

To evaluate the impact of sleeve gastrectomy on bone outcomes in adolescents and young adults over 12 months using dual energy X-ray absorptiometry (DXA) and high resolution peripheral quantitative computed tomography (HRpQCT).

Participants and methods

We enrolled 44 youth 14–22 years old with moderate to severe obesity; 22 underwent sleeve gastrectomy and 22 were followed without surgery (16 females and 6 males in each group). At baseline and 12 months, DXA was used to assess areal bone mineral density (aBMD), HRpQCT of the distal radius and tibia was performed to assess bone geometry, microarchitecture and volumetric BMD (vBMD), and finite element analysis to assess strength estimates (stiffness and failure load). These analyses were adjusted for age, sex, race and the bone measure at baseline. Fasting blood samples were assessed for calcium, phosphorus, and 25(OH) vitamin D (25OHD) levels.

Results

Over 12-months, the surgical group lost 27.2% of body weight compared to 0.1% in the non-surgical (control) group. Groups did not differ for changes in 25OHD levels (p = 0.186). Compared to controls, the surgical group had reductions in femoral neck and total hip aBMD Z-scores (p ≤ 0.0006). At the distal tibia, compared to controls, the surgical group had reductions in cortical area and thickness and trabecular number, and increases in trabecular area and separation (p ≤ 0.026). At the distal radius, the surgical group had greater reductions in trabecular vBMD, than controls (p = 0.010). The surgical group had an increase in cortical vBMD at both sites (p ≤ 0.040), possibly from a decrease in cortical porosity (p ≤ 0.024). Most, but not all, differences were attenuated after adjusting for 12-month change in BMI. Groups did not differ for changes in strength estimates over time, except that increases in tibial stiffness were lower in the surgical group (p = 0.044) after adjusting for 12-month change in BMI.

Conclusions

Over 12 months, weight loss associated with sleeve gastrectomy in adolescents had negative effects on areal BMD and certain HRpQCT parameters. However, bone strength estimates remained stable, possibly because of a simultaneous decrease in cortical porosity and increase in cortical volumetric BMD. Additional research is necessary to determine the relative contribution(s) of weight loss and the metabolic effects of surgery on bone outcomes, and whether the observed effects on bone stabilize or progress over time.

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.

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