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. Author manuscript; available in PMC: 2022 Aug 1.
Published in final edited form as: Bone. 2021 Apr 24;149:115975. doi: 10.1016/j.bone.2021.115975

Impact of sleeve gastrectomy on bone outcomes in adolescents vs. adults with obesity

Miriam A Bredella 1, Nazanin Hazhir Karzar 2, Vibha Singhal 2,3,4, Amita Bose 2, Abisayo Animashaun 2, Deborah M Mitchell 3,5, Elaine W Yu 5,*, Madhusmita Misra 2,3,*
PMCID: PMC8217278  NIHMSID: NIHMS1697015  PMID: 33901724

Abstract

Background:

Sleeve gastrectomy (SG) is the most common metabolic and bariatric surgery (MBS) procedure in adolescents and adults. Only few studies have assessed bone outcomes following SG and it is unknown whether skeletal changes differ by age group. Recent studies have identified marrow adipose tissue (MAT) as a novel biomarker for bone quality with studies in adults showing high MAT in those with visceral adiposity and a reciprocal increase in MAT with bone loss.

Objective:

To determine the impact of SG on volumetric BMD (vBMD) and MAT in adolescents and adults with obesity. We hypothesized that SG would lead to a decrease in vBMD and increase in MAT but that these changes would be less pronounced in adolescents compared to adults.

Materials and Methods:

The study was IRB-approved and HIPAA-compliant. Written informed consent/assent was obtained. We examined 10 adolescents (mean age 17.8±2.5 years, mean BMI 43.5±5.6 kg/m2) and 10 sex, race, and BMI-matched adults (mean age 49.5±13.6 years, mean BMI 43.7±5.9 kg/m2), before and 12 months after SG. At baseline and 12 months, subjects underwent quantitative CT of the lumbar spine (L1-L2) to assess trabecular vBMD, single voxel proton MR spectroscopy at 3T (PRESS pulse sequence without water suppression) at L1-L2 to quantify MAT, and MRI of the abdomen to assess visceral (VAT) and subcutaneous adipose tissue (SAT).

Results:

At baseline, adolescents had lower MAT (p=0.0002) and higher vBMD (p=0.050) compared to adults. Adolescents and adults lost 27.9±6.5 vs. 25.0±11.2% of body weight (p<0.0001 for within group change), while there was no significant difference between groups (p=0.455). There was a significant reduction in vBMD in adults (−3.9±3.9 %, p=0.005) and a trend for a reduction in adolescents (−3.7±7.5 %, p=0.119), with no significant difference between groups (p=0.944). Lumbar MAT content increased in both adults and adolescents (p≤0.034), while the difference was not significant between groups (p=0.281). In adolescents and adults, 12-month percent change in weight and BMI was positively associated with % change in MAT (p≤0.042). 12-month percent change in MAT was positively associated with 12-month % change in SAT in adolescents and 12-month percent change in VAT in adults (p≤0.045).

Conclusion:

SG in adolescents and adults with severe obesity is associated with a reduction in lumbar vBMD and an increase in lumbar MAT, although the reduction in adolescents did not reach statistical significance, with no significant differences in these endpoints between groups. Our results suggest detrimental effects of bariatric surgery on bone for patients across the life span.

Keywords: marrow adipose tissue (MAT), proton MR spectroscopy, sleeve gastrectomy, adolescents, adults, bone mineral density (BMD), quantitative computed tomography (QCT)

Introduction

The prevalence of obesity has increased over the last decades with an increase in severe obesity in adolescents and adults (1). Concomitantly, there has been a rise in metabolic and bariatric surgery (MBS) procedures, with sleeve gastrectomy (SG) being the most commonly performed procedure in adolescents and adults (2, 3). While MBS is very effective in treating cardiometabolic complications of obesity (4), it may have detrimental effects on the skeleton (5-9). Studies in adults and adolescents have indicated a reduction in bone mineral density (BMD) after SG (5, 10), and studies in adults have shown a higher fracture rate following MBS (11). Adolescence is the crucial time of maximal bone accrual towards attainment of peak bone mass, which is an important determinant of skeletal integrity (12), therefore, processes that affect bone accrual during adolescence might have negative consequences later in life.

A challenge in subjects undergoing SG is the accurate assessment of BMD before and after surgery. Dual energy x-ray absorptiometry (DXA) is the most commonly performed technique to assess BMD but is highly susceptible to extreme changes in soft tissue thickness, as is typically seen following SG (13). These challenges can in part be overcome by using quantitative computed tomography (QCT), a technique that measures volumetric BMD (vBMD) instead of areal BMD, and has a smaller error following extreme weight loss compared to DXA (14).

Recent studies have highlighted the unique role of marrow adipose tissue (MAT) in skeletal integrity and metabolic disease (15-18). Studies have suggested that MAT may contribute to bone fragility and fracture risk independent of BMD (19, 20). MAT is a dynamic compartment and changes with ageing. During adolescence, there is physiologic conversion of hematopoietic to fatty marrow (21), and further age-related increases in marrow adiposity are seen in older adults (22). In adolescents with obesity, MAT is inversely associated with VAT (23), while in adults with abdominal obesity, MAT is positively associated with VAT (17).

MAT also responds to nutritional challenges. For example, adults with anorexia nervosa have high MAT content of the lumbar spine (15) which decreases following recovery (24). Studies in adolescents (25) and adults (5) have shown an increase in MAT of the lumbar spine 12 months after SG, while a study examining adults 6 months after SG found no difference in MAT (26). Given the rapid changes in bone remodeling of the growing skeleton, MAT in adults and adolescents might respond differently to weight loss and changes in body composition, and adolescents might be able to better adapt to the detrimental effects of SG on the skeleton compared to adults.

Therefore, the purpose of this study was to determine the impact of SG on lumbar spine vBMD and MAT in adolescents and adults with severe obesity matched for sex and BMI. We hypothesized that SG would lead to a decrease in vBMD and increase in MAT but that these changes would be less pronounced in adolescents compared to adults.

Materials and Methods

Our study was IRB-approved and Health Insurance Portability and Accountability Act compliant. Written informed consent/assent was obtained from all subjects.

Subjects

Subjects with moderate-to-severe obesity (BMI of ≥35 kg/m2) scheduled to undergo SG were recruited from tertiary care obesity treatment centers. Subjects were participants of two clinical trials studying the effects of MBS on bone, and the study designs and a subset of the study subjects have been reported previously (5, 25). For this study, subjects were matched 1:1 by sex, race and within 2 kg/m2 for BMI between the adolescent and adult groups.

In brief, subjects were included for this study if they were anticipated to undergo SG and were between 14 to 21 years for the adolescent group (27) and age ≥ 25 years for the adult group. Exclusion criteria for both groups were pregnancy, history of medical disorders known to affect bone metabolism, use of bone-active medication (except for calcium and vitamin D supplementation), history of smoking more than ten cigarettes per day or of substance abuse (per DSM-5), weight >200 kg (due to limitations of the MRI scanner) and contraindications to MRI, such as the presence of a metallic implant or claustrophobia.

Study subjects underwent a history and physical examination, fasting blood tests, QCT and proton MR spectroscopy (1H-MRS) of the lumbar spine, and MRI of the abdomen to assess body composition at baseline prior to SG and 12 months after SG. All participants were offered at least 1200 mg elemental calcium and 800 IUs vitamin D daily to optimize calcium intake and absorption with additional recommendations as previously described (10).

Quantitative Computed Tomography (QCT)

Volumetric bone mineral density (vBMD) of the lumbar spine (L1-L2) was assessed using a 16-multidetector-row CT scanner (LightSpeed Pro, GE Healthcare, Waukesha, WI, USA) with the use of a calibration phantom and analyzed using QCTPro software (Mindways Software, Inc., Austin, TX, USA), as previously described (5, 25, 28).

Proton Magnetic Resonance Spectroscopy

Subjects underwent single voxel proton Magnetic Resonance spectroscopy (1H-MRS) of the 1st and 2nd lumbar vertebrae (L1-L2) on a 3.0 Tesla MR imaging system (Siemens Trio; Siemens Medical Systems, Erlangen, Germany) using a point-resolved spatially localized spectroscopy (PRESS) pulse sequence without water suppression after an overnight fast as previously described (5, 25). Fitting of 1H-MRS data was performed using LC Model (version 6.3-0K, Stephen Provencher, Oakville, Canada). Lipid resonances were scaled to unsuppressed water peak (4.7 ppm) and expressed in lipid-to-water ratios (LWR).

Magnetic Resonance Imaging

Single slice MRI (Siemens Trio; Siemens Medical Systems, Erlangen, Germany) was performed at the midportion of the 4th lumbar vertebra (L4) to determine abdominal adipose tissue depots using a T1-weighted fast spin-echo pulse sequence, and visceral adipose tissue (VAT) and abdominal subcutaneous adipose tissue (SAT) compartment cross-sectional areas (cm2) were determined (VITRAK, Merge/eFilm, Milwaukee, WI) as previously described (5, 25).

Calcium and vitamin D

Fasting calcium and 25(OH)vitamin D (25OHD) (intra- and interassay coefficients of variation ≤ 3%) (LabCorp, Burlington, NC, USA) were assessed.

Statistical Analysis

Statistical analyses were performed using JMP Statistical Discovery Software (Version 12, SAS Institute, Carey, NC). Baseline characteristics and 12-month percent changes before and after SG between the adult and adolescent groups were compared by Student’s t-test or the Wilcoxon Rank Sum test depending on the data distribution. 12-month changes before and after SG within adolescents and adults were assessed using paired t-tests or Wilcoxon sign rank test. Linear regression analysis was performed to determine the correlations between change in weight and body composition and change in lumbar vBMD and MAT. Pearson correlation coefficients are reported. P ≤ 0.05 was used to denote significance. Data are presented as mean ± SD. This was a secondary analysis of a matched sample from two studies; therefore, no power calculation was performed for this preliminary investigation.

Results

Baseline Characteristics

The study group included 10 adolescents (mean age 17.8±2.5 years, range 14 to 21 years; mean BMI 43.5±5.6 kg/m2, range 38.3 to 55.7 kg/m2) and 10 sex, race, and BMI-matched adults (mean age 49.5±13.6 years, range 25 to 65 years; mean BMI 43.7±5.9 kg/m2, range 35.5 to 55.8 kg/m2), who underwent SG. Each group included 9 females and 1 male, and 4 Black and 6 White participants. Subject characteristics, body composition, and bone parameters are shown in Table 1. Adolescents had higher SAT, lower VAT, higher vBMD, and lower MAT compared to adults. Clinical characteristics, bone, and body composition parameters have been previously reported in a subset of subjects (5, 25), however, no comparison between adults and adolescents has been performed.

Table 1.

Effects of sleeve gastrectomy on body composition and bone outcomes in adolescents vs. adults 12 months after surgery

Variable Group Baseline 12 months 12-month %
change		 p-value
within group		 p-value 12-
month change
between
groups
Weight (kg) adolescents 124.1 ± 20.8 89.2 ± 14.6 −27.9 ± 6.5 <.0001 0.455
adults 113.7 ± 17.6 85.7 ± 20.3 −25.0 ± 10.1 <.0001
BMI (kg/m2) adolescents 43.5 ± 5.6 31.1 ± 4.5 −28.2 ± 6.6 0.002 0.520
adults 43.7 ± 5.9 32.6 ± 7.2 −25.5 ± 11.2 <.0001
Serum calcium (mg/dl) adolescents 9.2 ± 0.3 9.2 ± 0.3 −0.8 ± 2.7 0.343 0.601
adults 9.6 ± 0.5 9.6 ± 0.3 0.2 ± 5.5 1.000
Serum 25-hydoxyvitamin D (ng/ml) adolescents 23.7 ± 7.0 26.3 ± 11.5 12.2 ± 30.7 0.566 0.258
adults 31.2 ± 12.7 41.7 ± 16.1 48.3 ± 82.1 0.095
Visceral adipose tissue (cm2) adolescents 119.2 ± 59.5* 60.1 ± 27.0 −46.5 ± 13.9 0.001 0.762
adults 203.8 ± 111.9 109.0 ± 70.4 −43.2 ± 29.5 0.013
Subcutaneous adipose tissue (cm2) adolescents 667.6 ± 152.4** 373.8 ± 161.6 −44.7 ± 17.3 <.0001 0.815
adults 502.3 ± 103.5 344.1 ± 209.8 −47.1 ± 24.9 0.003
L1-L2 vBMD (mg/cm3) adolescents 201.7 ± 26.1* 193.9 ± 25.9 −3.7 ± 7.5 0.119 0.944
adults 167.0 ± 45.5 160.6 ± 44.9 −3.9 ± 3.9 0.005
L1-L2 MAT (LWR) adolescents 0.27 ± 0.12 *** 0.36 ± 0.19 38.8 ± 44.2 0.025 0.281
adults 0.86 ± 0.34 1.05 ± 0.46 20.5 ± 26.9 0.034
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Abbreviations: BMI, body mass index; vBMD, volumetric bone mineral density; MAT, marrow adipose tissue; LWR, lipid to water ratio

*

P value =0.05 for differences between adolescents and adults at baseline

**

P value <0.05 for differences between adolescents and adults at baseline

***

P value <0.001 for differences between adolescents and adults at baseline

Effects of bariatric surgery on weight and body composition

Changes in weight and body composition before and 12 months after SG are shown in Table 1. Adolescents lost −27.9± 6.5% of total body weight and adults lost −25.0 ± 10.1% of total body weight (p<0.0001 within each group) and this change did not differ between groups (p=0.455). Both groups lost VAT and SAT (p≤0.013 within each group) but the change did not differ significantly between groups (p≥0.762).

Effects of bariatric surgery on bone outcomes

Among adults, we observed a 3.9% reduction in lumbar spine vBMD (p=0.005) in the 12 months following SG. We observed a similar magnitude though not statistically significant reduction of spine vBMD in adolescents (−3.7% ± 7.5, p=0.119). There was no between-group difference in percent vBMD loss (p=0.944). Despite lower baseline MAT among adolescents, both adolescents and adults experienced statistically significant increases in MAT following SG (adolescents: 38.8% ± 44.2, p=0.025; adults: 20.5% ± 26.9, p=0.034), which did not differ between groups (p=0.281).

Mean serum calcium and 25(OH) vitamin D did not change significantly within or between groups and were within the normal range in both groups at 12 months (Table 1).

Correlations between body composition and bone outcomes

Among both adolescents and adults, 12-month percent change in MAT was positively associated with percent change in both weight and BMI, indicating that greater increases in MAT were observed among those who lost less body weight after SG. Additionally, 12-month percent change in MAT was positively associated with percent change in VAT among adults and with percent change in SAT among adolescents (Table 2).

Table 2.

Pairwise Correlation of 12-Month % Changes in Body Composition and Bone Outcomes in Adolescents and Adults after sleeve gastrectomy

Variable 12-month % change vBMD 12-month % change MAT
12-month % change r p-value r p-value
Weight
 Adolescents −0.514 0.128 0.730 0.016
 Adults 0.195 0.588 0.649 0.042
BMI
 Adolescents −0.563 0.089 0.708 0.021
 Adults 0.176 0.626 0.634 0.048
Visceral adipose tissue
 Adolescents −0.344 0.329 −0.219 0.542
 Adults 0.145 0.708 0.740 0.022
Subcutaneous adipose tissue
 Adolescents −0.642 0.045 0.648 0.042
 Adults −0.432 0.332 0.630 0.128
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Abbreviations: BMI, body mass index; vBMD, volumetric bone mineral density; MAT, marrow adipose tissue; LWR, lipid to water ratio

Among adolescents, 12-month percent change in spine vBMD was inversely associated with percent change in SAT, indicating that lesser loss of vBMD was seen among those with greater loss of SAT. We did not observe significant correlations of vBMD changes with changes in other body composition parameters (Table 2).

There was no significant correlation between 12-month percent change in spine BMD and 12-month percent change in lumbar MAT in adolescents or adults (p>0.05).

Discussion

Our study demonstrates that, among adolescents and adults with moderate to severe obesity, SG leads to decreases in lumbar vBMD and increases in lumbar MAT of similar magnitude over 12 months. Change in MAT is associated with change in SAT in adolescents and with change in VAT in adults. Our study confirms detrimental effects of SG on bone for patients across the life span.

MBS, including SG (currently the most commonly performed MBS in adults and adolescents), has negative effects on the skeleton (5, 10). Skeletal integrity is determined not only by BMD but also its microenvironment and we have previously shown increases in MAT of the lumbar spine 12 months after SG in both adolescents (25) and adults (5).

The impact of SG on the skeleton may differ by age. Adolescence is the time of maximal bone accrual towards attainment of peak bone mass (12), and processes that affect bone during this important period might have sequelae on bone health later in life. However, ongoing bone anabolism during adolescence might enable better adaptation to the damaging effects of SG on the skeleton. We therefore compared the effects of SG on BMD and MAT in adults and adolescents and hypothesized that these changes would be less pronounced in adolescents compared to adults.

At baseline, adults had higher MAT of the lumbar spine compared to adolescents of similar sex and BMI, consistent with the physiologic conversion of hematopoietic to fatty marrow with age (21). Adults also had lower baseline vBMD compared to adolescents, consistent with known reductions in BMD during ageing. Of note, the percent difference in baseline MAT was larger compared to the difference in baseline vBMD between the groups, suggesting that these compartments function independently. Furthermore, at similar BMI, adults had higher VAT and adolescents had higher SAT, suggesting that the obese state leads to different physiologic changes between these groups. These findings are consistent with a study by Linder et al (29) that found lower VAT in adolescents compared to BMI and sex-matched adults with obesity. Despite these baseline differences in body composition, we found similar reductions in weight and BMI, 12 months after SG in adults and adolescents. In addition, the reductions in VAT and SAT were similar within both groups without significant difference between groups. SG was not associated with significant changes in calcium and vitamin D, as both groups received calcium and vitamin D supplementation.

We had hypothesized that changes in BMD and MAT after SG would be less pronounced in adolescents compared to adults, due to ongoing bone anabolism during adolescence that might enable better adaptation to the damaging effects of SG on the skeleton. Contrary to this hypothesis, SG led to a significant reduction of lumbar spine vBMD after 12 months in adults and a similar trend in adolescents, with no significant difference between groups. A reason why the 12-month change in adolescents was only a trend might be due to the small sample size or because the skeleton in adolescents was able to better adapt to the damaging effect of SG. MAT of the lumbar spine increased in both groups with no difference in the magnitude of 12-month change between the groups. These results suggest that SG has similar consequences to the skeleton in both adults and adolescents. Interestingly, these findings are in contrast with changes in MAT after Roux-en-Y gastric bypass, another form of MBS which appears to either not change or to slightly decrease MAT (5, 30, 31). The physiologic underpinnings of these differential effects by bariatric surgery procedure are unknown.

Finally, we performed exploratory analyses to evaluate whether changes in MAT could be explained by changes in body composition. We found positive correlations between 12-month change in MAT and 12-month change in weight and BMI in adolescents and adults, which indicates that MAT increases are greatest among patients who lost the least amount of body weight. This seems counterintuitive, and be related to bone marrow response to the different phases of starvation, with an initial increase in MAT which then decreases and can lead to serous atrophy of bone marrow (32-34). However, this is hypothetical as we did not perform studies to examine different phases of starvation and did not examine the skeleton for serous atrophy. We also documented a positive correlation between 12-month change in MAT and SAT in adolescents and a positive correlation between 12-month change in MAT and VAT in adults, consistent with the known positive correlation between MAT and VAT in adults (17).

Our study had several limitations, the most important one being our relatively small sample size which increases the risk of a type 2 error. We were able to detect differences in vBMD and MAT within groups but not between groups. It will be important to perform larger and longer follow-up studies to assess whether differences will become apparent as time since procedure lengthens. Strengths of our study include the assessments of adults and adolescents using advanced imaging techniques, such as QCT to determine vBMD, which is less susceptible to extreme changes in body composition after MBS, and 1H-MRS to assess MAT content and MRI to assess abdominal fat compartments.

In conclusion, SG in adolescents and adults with moderate to severe obesity is associated with a reduction in lumbar vBMD and an increase in MAT, with no significant differences in these endpoints between groups. Change in MAT was positively associated with change in SAT in adolescents and with change in VAT in adults. Our results confirm detrimental effects of SG on bone in adolescents and adults, and suggest differential effects of MAT on abdominal fat depots. Longer follow-up studies will be required to assess the progression of these changes and to what extent they increase fracture risk.

Highlights.

  • Adolescents have lower lumbar marrow adipose tissue (MAT) compared to adults

  • Sleeve gastrectomy (SG) causes similar reductions in vBMD in adolescents and adults

  • SG increases MAT in adolescents and adults

  • SG has detrimental effects on bone for patients across the life span

Acknowledgments

Grant support: This work was supported by the following grants: NIH NIDDK R01 DK103946-01A1 (MM, MAB), NIH K23DK110419-01 (VS), K24DK109940 (MAB), K24 HD071843 (MM), NIH P30-DK057521 (VS). P30 DK040561, R03 DK107869 (EY) L30 DK089544 (EY), K23 DK093713 (EY), UL1 TR001102

Footnotes

Disclosures: The authors do not have any conflicts of interests to disclose.

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