Abstract
Objective: Dual energy X-ray absorptiometry (DXA) was used to analyze body composition, bone mineral density (BMD) parameters and the trabecular bone score (TBS) in patients with obesity before, 3 months after and 1 year after bariatric surgery as a method to evaluate the changes in BMD and skeletal microarchitecture (MA) in patients with obesity after bariatric surgery and to provide a basis for further accurate assessment of the bone health status of this population and subsequent treatment. Methods: This study was a retrospective analysis of 41 patients that underwent DXA imaging before, 3 months after and maximum 1 year after bariatric surgery. The follow-up rate in both periods was 100%. First, the changes in BMD and TBS before and after surgery were compared between patients grouped by sex and obesity degree. Secondly, the correlations between the TBS or BMD and body composition 1 year after surgery were analyzed. Results: The BMD and TBS were within the normal range after bariatric surgery. Changes in the BMD and TBS were related to time, the degree of obesity and sex. Changes in the TBS were closely related to changes in the BMD, and the trends in the changes in the BMD were basically the same among the different groups of individuals with obesity of different sexes. A negative correlation was observed between the TBS and fat percentage (total body, leg, trunk, android area), as well as the lumbar spine Z-score in patients 1 year after bariatric surgery (p < 0.05). Conclusions: Bariatric surgery in patients with obesity has no obvious adverse effects on BMD or TBS. DXA can be used to better evaluate the changes in BMD and MA in patients with obesity after bariatric surgery, providing a basis for the clinical evaluation of post-bariatric surgery efficacy in these individuals and subsequent accurate assessment of the bone health status and treatment of this population.
Keywords: Bariatric surgery, Bone mineral density, Body composition, Trabecular bone score, Skeletal microarchitecture
Subject terms: Diseases, Endocrinology, Health care, Medical research, Risk factors
Introduction
Significant changes in body composition and distribution occur in patients with obesity after bariatric surgery, and dual energy X-ray absorptiometry (DXA) measurements can provide many references for the evaluation of postoperative efficacy and the prevention of complications. In addition to concerns about changes in body composition resulting from weight loss surgery, the impact of weight loss surgery on bone health is becoming increasingly concerning, and people are beginning to worry about the adverse effects of weight loss on bone health, such as bone loss, increased fragility, and even an increased risk of fracture after weight loss surgery1.
Bone mineral density (BMD), which is based on DXA measurements, is the primary measure for assessing bone strength and fracture risk. However, studies have shown that approximately 50% of clinical fractures in women with no osteoporosis (i.e., those with BMD T value > -2.5), are diagnosed according to BMD2. Even in patients with type 2 diabetes (T2DM), the BMD is often greater than normal, but the risk of fracture is increased, mainly due to decreased bone quality, especially the destruction of skeletal microarchitecture (MA)3. Moreover, the BMD of most patients with fragility fractures is characterized only as bone mass loss or even within the normal range, suggesting that the protection of bone structure quality is more important than the protection of bone mass4. DXA can only be used to evaluate bone mass and cannot reflect changes in MA or evaluate bone quality; thus, limitations exist in the diagnosis of osteoporosis and the assessment of fracture risk. Therefore, a noninvasive tool to evaluate MA, the trabecular bone score (TBS), was developed.
Developed abroad in recent years, the TBS is an indicator that reflects the microstructure of bone trabeculae and is a powerful tool for evaluating bone quality and predicting fracture risk5–8. TBS is calculated by computer software (TBS iNsight software) that analyzes the grayscale variation level of lumbar BMD images and MA scores, such as the number of bone trabeculae and space size, which can predict fracture risk independently of BMD and is not affected by lumbar osteoarthritis9–12. The higher the TBS, the stronger the microsystem structure; and the lower the TBS, the worse the bone quality and the greater the susceptibility to fracture. Using the TBS to assess bone MA changes and fracture risk after bariatric surgery may be feasible; however, to date, limited data are available for this population, and no studies have assessed the Chinese population. In this context, the objective of our study was to assess bone MA changes by measuring BMD parameters and the TBS at 3 months and 1 year after bariatric surgery in a Chinese population and to numerically analyze the influence of body composition on the TBS. This study provides a basis for the clinical evaluation of the postoperative effect of weight loss on patients with obesity and the subsequent accurate evaluation of skeletal health status and treatment.
Materials and methods
Subject information
Patients who underwent bariatric surgery and DXA bone mineral density measurements in the Department of Nuclear Medicine of the First Affiliated Hospital of Jinan University from June 2017 to December 2022 were retrospectively analyzed. The inclusion criteria included the following:
(1) Patients who underwent bariatric surgery;
(2) DXA scans of the lumbar spine and proximal femur were performed at least once before surgery (within one week), 3 months after surgery, and 1 year after surgery;
(3) The TBS can be calculated.
The exclusion criteria included the following:
(1) Acute severe cardiovascular events occurring within 6 months;
(2) Recent coinfection;
(3) Patients with a history of malignant tumors;
(4) Patients who received anti-inflammatory drug therapy and hormone replacement therapy;
(5) Patients with diseases that affect calcium or bone metabolism.
According to the inclusion and exclusion criteria listed above, a total of 41 patients (17 males and 24 females) underwent three consecutive DXA re-examinations before, 3 months after and 1 year after bariatric surgery.
Definition of obesity, BMD and TBS
According to different fat accumulation sites, obesity can be divided into peripheral obesity and central obesity13. Currently, body mass index (BMI) is used to diagnose overweight or obesity, and waist circumference is used to diagnose central obesity. According the World Health Organization (WHO)’s guidelines on BMI, obesity level is classified as overweight (25.0–29.9 kg/m2), first-degree obesity (30–34.9 kg/m2), second-degree obesity (35.0–39.9 kg/m2), and third-degree obesity (≥ 40.0 kg/m2).
BMD is commonly used to indicate bone mass in clinical practice. For postmenopausal women and men aged 50 years or older, the use of a T score for the same race is recommended to determine the BMD level. It is recommended to use the BMD of the axial skeleton (lumbar vertebrae 1‒4, femoral neck or whole hip) or a bone density-related T score of the distal 1/3 of the radius ≤ -2.5 measured by DXA as the diagnostic criterion for osteoporosis. For children, premenopausal women and men younger than 50 years of age, the Z score is recommended to determine their BMD level, and a Z score ≤ -2.0 is recommended as the diagnostic criterion for low bone mass14.
According to international prospective studies15, the criteria for a TBS are as follows: a TBS (L1–L4) greater than or equal to 1.31 indicates a low risk of fracture, and the MA is normal; the TBS ranges from 1.31 to -1.23, suggesting moderate fracture risk and partial MA impairment. If the TBS value is less than or equal to 1.23, the MA is obviously damaged. Based on the definition of osteoporosis by BMD, Gong Jian et al.16 determined the peak value of the TBS and its critical value for low bone mass and established the TBS criteria for Chinese men and women; for Chinese men, a TBS (L1–L4) ≥ 1.39 indicates normal MA, a TBS of 1.31–1.39 is partial MA impairment, and a TBS ≤ 1.31 is MA impairment. In Chinese women, a TBS ≥ 1.35 indicates normal MA, a TBS of 1.27–1.35 indicates partial MA impairment, and a TBS ≤ 1.27 indicates MA impairment.
Measurement of body composition and BMD
DXA was used to measure the body composition of the patients before and after bariatric surgery. The measuring instrument used was LUNAR iDXA produced by GE, and the analysis software used was enCORE (version 16).
The main DXA measurement site was the axial skeleton, including the lumbar spine and proximal femur. The BMDs of L1–L4, the femoral neck and the total hip were measured with the subjects in the anterior position. The results are presented as g/cm2, and the collected data were sent to a BMD workstation for analysis.
As the patients in this study were premenopausal women and men under 50 years of age, the BMDs and Z scores of the lumbar spine (L1–L4), femoral neck and total hip were recorded before and after bariatric surgery. The parameters of the body composition measurement and analysis included the body bone mineral content (BMC), total body and local (arms, legs, trunk, android area, and gynoid area) fat mass (FM), lean mass (LM), fat percentage of body fat mass (fat%), visceral adipose tissue mass (VAT mass), visceral adipose tissue volume (VAT volume), and body composition index and distribution parameters.
Calculation of the TBS
TBS iNsight Software (TBS iNsight Software, 3.0.2.0, Med-Imaps, France) was used to analyze the grayscale variation level of lumbar vertebra bone density images (L1–L4 bone density) obtained via DXA, calculate the TBS value, and evaluate MA.
Agustina et al.17 divided TBS results into “All TBS Values” (including all patients, regardless of BMI) and “Strict TBS Values” (including only patients with a BMI of 15 kg/m2–37 kg/m2). All DXA scans were performed by an experienced technical operator. All the DXA scans were reviewed by two senior attending physicians.
Precision of DXA Bone Density and the TBS
In this research center18, 30 healthy volunteers were repeatedly measured via DXA to evaluate the precision of the instrument. The precision of the instrument was represented by the root mean square of the coefficient of variation (RMS-CV%). The BMD (L1–4) and TBS (L1–4) were < 0.7% and 0.1%, respectively.
Statistical analysis
All the research data were processed using SPSS 25.0 statistical software and plotted with GraphPad Prism 8.0 software. The quantitative data are presented as the means ± standard deviations (
± s). The Kolmogorov‒Smirnov test was used to test the normality of the variables. A paired t test was used for the samples meeting the normal distribution of the two pairs, the Wilcoxon signed rank sum test was used for the samples not meeting the normal distribution, and the Friedman test was used for the samples from multiple pairs. For the analysis of correlations among parameters, Pearson’s correlation analysis was used for variables with a normal distribution, Spearman’s correlation analysis was used for variables with an abnormal distribution, and curve fitting was performed for variables with significant differences in the correlation analysis. p < 0.05 indicates that the difference is statistically significant.
Results
Results of the BMD and TBS before, 3 months after and 1 year after bariatric surgery
BMD and TBS before, 3 months after and 1 year after bariatric surgery (Table 1)
Table 1.
Results of BMD and TBS before, 3 months and 1 year after bariatric surgery(
± s ).
| Variable | before surgery | 3 months after surgery | 1 year after surgery |
|---|---|---|---|
| BMI(kg/m2) | 40.50 ± 4.21 | 28.42 ± 5.57* | 24.49 ± 3.10**# |
| Femoral neck | |||
| BMD (g/cm2) | 1.071 ± 0.142 | 1.083 ± 0.130 | 1.010 ± 0.122**# |
| Z-Score | 0.17 ± 0.90 | 0.45 ± 0.83 | 0.33 ± 0.74 |
| Total hip | |||
| BMD (g/cm2) | 1.131 ± 0.13 | 1.123 ± 0.13 | 1.064 ± 0.124**# |
| Z-Score | 0.49 ± 0.95 | 0.55 ± 0.98 | 0.26 ± 0.73 |
| Lumbar spine | |||
| BMD (g/cm2) | 1.241 ± 0.08 | 1.241 ± 0.10 | 1.273 ± 0.112 |
| Z-Score | 0.14 ± 1.22 | 0.67 ± 0.95 | 0.98 ± 0.77# |
| All TBS Values | 1.50 ± 0.08 | 1.47 ± 0.09* | 1.40 ± 0.11**# |
| Strict TBS Values | -- | 1.47 ± 0.10 | 1.40 ± 0.11** |
* p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
The results revealed that the BMD of the proximal femur (femoral neck, total hip) decreased significantly 1 year after bariatric surgery (p < 0.05) and that the BMD of the lumbar spine was not significantly changed after bariatric surgery. A significant decrease in the TBS was observed 1 year after bariatric surgery (p < 0.05). The BMD and TBS were within the normal range after bariatric surgery.
BMD and TBS before, 3 months after and 1 year after bariatric surgery in patients with different degrees of obesity (Table 2)
Table 2.
Results of BMD and TBS before, 3 months and 1 year after bariatric surgery in patients with different obesity degrees(
± s ).
| Variable | First degree obesity(n = 2) | Second degree obesity(n = 19) | Third degree obesity(n = 20) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | |
| BMI(kg/m2) | 34.85 ± 0.07 | 30.20 ± 0.14 | 25.20 ± 4.53 | 37.81 ± 1.60 | 26.95 ± 4.22* | 23.23 ± 2.48# | 43.62 ± 3.76 | 29.65 ± 6.83* | 25.81 ± 3.19# |
| Femoral neck | |||||||||
| BMD (g/cm2) | 0.95 ± 0.19 | 0.95 ± 0.17 | 0.95 ± 0.17 | 1.05 ± 0.13 | 1.04 ± 0.11 | 1.00 ± 0.12**# | 1.11 ± 0.14 | 1.12 ± 0.13 | 1.04 ± 0.12**# |
| Z-Score | -0.12 ± 0.71 | 0.03 ± 0.42 | 0.03 ± 0.42 | -0.14 ± 0.77 | 0.35 ± 0.83 | 0.30 ± 0.64# | 0.48 ± 0.95 | 0.58 ± 0.86 | 0.41 ± 0.89 |
| Total hip | |||||||||
| BMD (g/cm2) | 1.00 ± 0.11 | 0.96 ± 0.07 | 0.95 ± 0.06 | 1.10 ± 0.09 | 1.08 ± 0.10 | 1.06 ± 0.10**# | 1.17 ± 0.14 | 1.16 ± 0.15 | 1.07 ± 0.14# |
| Z-Score | 0.04 ± 0.47 | -0.05 ± 0.21 | -0.18 ± 0.06 | 0.04 ± 0.61 | 0.10 ± 0.79 | 0.15 ± 0.55 | 0.92 ± 1.05 | 0.89 ± 0.99 | 0.44 ± 0.89 |
| Lumbar spine | |||||||||
| BMD (g/cm2) | 1.35 ± 0.21 | 1.23 ± 0.16 | 1.06 ± 0.07 | 1.24 ± 0.10 | 1.25 ± 0.11 | 1.32 ± 0.08 | 1.23 ± 0.07 | 1.22 ± 0.10 | 1.22 ± 0.13 |
| Z-Score | 1.25 ± 0.36 | 1.19 ± 0.34 | 1.04 ± 0.37 | 0.13 ± 1.65 | 0.60 ± 1.08 | 1.07 ± 0.79# | 0.15 ± 0.85 | 0.69 ± 0.87 | 0.87 ± 0.79 |
| All TBS Values | 1.40 ± 0.07 | 1.38 ± 0.04 | 1.34 ± 0.01 | 1.50 ± 0.08 | 1.49 ± 0.08 | 1.40 ± 0.11# | 1.52 ± 0.09 | 1.45 ± 0.10 | 1.40 ± 0.12# |
| Strict TBS Values | 1.38 ± 0.04 | 1.34 ± 0.01 | 1.49 ± 0.08 | 1.40 ± 0.11** | 1.45 ± 0.10 | 1.40 ± 0.12** | |||
* p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
The average preoperative BMI of the 2 patients in the first-degree obesity group was 34.85 ± 0.07 kg/m2. The average preoperative BMI of the 19 patients in the second-degree obesity group was 37.81 ± 1.60 kg/m2. The average preoperative BMI of the 20 patients in the third-degree obesity group was 43.62 ± 3.76 kg/m2. The data from 2 patients in the first-degree obesity group were not statistically analyzed. The results revealed that the BMD and TBS of the two groups of patients with obesity were within the normal range 3 months after and 1 year after bariatric surgery. BMD (femoral neck, total hip) and the TBS in the second- and third-degree obesity groups did not decrease significantly 3 months after surgery but did decrease significantly 1 year after surgery (p < 0.05). Significant changes in lumbar BMD were not observed in the three obese groups after the operation. The BMD and TBS showed the same trend of postoperative changes in the different obesity groups (Fig. 1).
Fig. 1.
Changes of BMD and TBS before, 3 months and 1 year after bariatric surgery in different obesity degree groups. A: femoral neck BMD B total hip BMD C lumbar spine BMD D TBS Values. * p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
BMD and TBS before, 3 months after and 1 year after bariatric surgery in male groups with different degrees of obesity (Table 3)
Table 3.
Results of BMD and TBS before, 3 months and 1 year after bariatric surgery in male groups with different obesity degrees(
± s ).
| Variable | First degree obesity(n = 1) | Second degree obesity(n = 4) | Third degree obesity(n = 13) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | |
| BMI(kg/m2) | 34.90 | 30.10 | 28.40 | 37.35 ± 1.89 | 25.33 ± 4.20 | 23.78 ± 2.58 | 43.12 ± 2.18 | 26.35 ± 3.03* | 25.35 ± 3.06# |
| Femoral neck | |||||||||
| BMD (g/cm2) | 1.09 | 1.07 | 1.07 | 1.09 ± 0.16 | 1.08 ± 0.14 | 1.01 ± 0.14 | 1.12 ± 0.13 | 1.12 ± 0.15 | 1.03 ± 0.12# |
| Z-Score | 0.38 | 0.33 | 0.33 | 0.33 ± 0.76 | 0.66 ± 0.57 | 0.14 ± 0.41 | 0.71 ± 0.87 | 0.72 ± 0.90 | 0.39 ± 0.84** |
| Total hip | |||||||||
| BMD (g/cm2) | 1.07 | 1.01 | 0.99 | 1.16 ± 0.10 | 1.13 ± 0.12 | 1.05 ± 0.11# | 1.18 ± 0.12 | 1.14 ± 0.12 | 1.09 ± 0.13 |
| Z-Score | 0.37 | 0.10 | -0.22 | 0.91 ± 0.34 | 0.55 ± 0.27 | 0.21 ± 0.53 | 1.28 ± 0.90 | 1.05 ± 0.92 | 0.65 ± 0.73 |
| Lumbar spine | |||||||||
| BMD (g/cm2) | 1.50 | 1.34 | 1.10 | 1.35 ± 0.19 | 1.26 ± 0.14 | 1.11 ± 0.20 | 1.21 ± 0.07 | 1.22 ± 0.08 | 1.16 ± 0.12 |
| Z-Score | 1.50 | 1.43 | 1.30 | 1.75 ± 0.89 | 1.26 ± 0.60 | 1.24 ± 0.91 | 0.40 ± 0.75 | 0.65 ± 0.85 | 0.60 ± 0.67 |
| All TBS Values | 1.45 | 1.40 | 1.33 | 1.52 ± 0.08 | 1.51 ± 0.09 | 1.47 ± 0.09 | 1.54 ± 0.07 | 1.45 ± 0.10 | 1.44 ± 0.07# |
| Strict TBS Values | 1.40 | 1.33 | 1.51 ± 0.09 | 1.47 ± 0.09 | 1.45 ± 0.10 | 1.44 ± 0.07** | |||
* p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
The preoperative BMI of 1 patient in the first-degree obesity group was 34.90 kg/m2. The average preoperative BMI of the 4 patients in the second-degree obesity group was 37.35 ± 1.89 kg/m2. The average preoperative BMI of the 13 patients in the third-degree obesity group was 43.12 ± 2.18 kg/m2.
The data from 1 patient in the first-degree obesity group were not statistically analyzed. The postoperative BMD and TBS in the two obese groups were within the normal range. The BMD and TBS in the second- and third-degree obesity groups did not significantly decrease 3 months after the operation; in the second-degree obesity group, only the BMD of the whole hip decreased significantly one year after surgery (p < 0.05). The BMD and TBS of the femoral neck of the three groups significantly decreased one year after surgery (p < 0.05). A significant change in lumbar BMD was not detected 1 year after surgery in the three obese groups (Fig. 2).
Fig. 2.
Changes of BMD and TBS before, 3 months and 1 year after bariatric surgery in men with different degrees of obesity. A: femoral neck BMD B total hip BMD C lumbar spine BMD D TBS Values. * p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
BMD and TBS before, 3 months after and 1 year after bariatric surgery in female groups with different degrees of obesity (Table 4)
Table 4.
Results of BMD and TBS before, 3 months and 1 year after bariatric surgery in female groups with different obesity degrees(
± s ).
| Variable | First degree obesity(n = 1) | Second degree obesity(n = 15) | Third degree obesity(n = 7) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | before surgery | 3 months after surgery | 1 year after surgery | |
| BMI(kg/m2) | 34.80 | 30.03 | 22.00 | 37.93 ± 1.57 | 27.55 ± 4.26 | 23.07 ± 2.53# | 44.53 ± 5.80 | 38.73 ± 6.12 | 26.82 ± 3.61# |
| Femoral neck | |||||||||
| BMD (g/cm2) | 0.82 | 0.83 | 0.83 | 1.04 ± 0.13 | 1.03 ± 0.11 | 1.00 ± 0.11 | 1.09 ± 0.16 | 1.14 ± 0.10 | 1.05 ± 0.15 |
| Z-Score | -0.62 | -0.27 | -0.27 | -0.24 ± 0.75 | 0.26 ± 0.88 | 0.34 ± 0.69# | -0.01 ± 1.00 | 0.32 ± 0.79 | 0.47 ± 1.15 |
| Total hip | |||||||||
| BMD (g/cm2) | 0.92 | 0.91 | 0.91 | 1.09 ± 0.09 | 1.07 ± 0.09 | 1.06 ± 0.10 | 1.16 ± 0.17 | 1.22 ± 0.19 | 1.02 ± 0.16 |
| Z-Score | -0.29 | 0.20 | -0.14 | -0.14 ± 0.49 | -0.01 ± 0.85 | 0.13 ± 0.58 | 0.26 ± 1.03 | 0.53 ± 1.18 | 0.05 ± 1.12 |
| Lumbar spine | |||||||||
| BMD (g/cm2) | 1.20 | 1.12 | 1.01 | 1.24 ± 0.11 | 1.25 ± 0.11 | 1.31 ± 0.08 | 1.30 ± 0.01 | 1.24 ± 0.14 | 1.35 ± 0.05 |
| Z-Score | 0.99 | 0.94 | 0.78 | 0.03 ± 1.76 | 0.39 ± 1.13 | 1.02 ± 0.78# | -0.86 ± 0.09 | 0.78 ± 0.97 | 1.35 ± 0.83 |
| All TBS Values | 1.36 | 1.35 | 1.34 | 1.49 ± 0.08 | 1.48 ± 0.08 | 1.38 ± 0.11# | 1.47 ± 0.1 | 1.45 ± 0.11 | 1.35 ± 0.15 |
| Strict TBS Values | 1.35 | 1.34 | 1.48 ± 0.08 | 1.38 ± 0.11** | 1.44 ± 0.13 | 1.35 ± 0.15 | |||
* p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
The preoperative BMI of 1 patient in the first-degree obesity group was 34.80 kg/m2. The average preoperative BMI of the 15 patients in the second-degree obesity group was 37.93 ± 1.57 kg/m2. The average preoperative BMI of the 7 patients in the third-degree obesity group was 44.53 ± 5.80 kg/m2.
The data for 1 patient in the first-degree obesity group were not statistically analyzed; the postoperative BMD and TBS in the two obese groups were within the normal range. No significant changes in the BMD or TBS were observed in the third-degree obesity group. The BMD in the second-degree obesity group did not decrease significantly after surgery, but it decreased significantly 1 year after TBS surgery (p < 0.05). The changes in the BMD and TBS differed between the second-degree obesity group but remained consistent between the third-degree obesity group after bariatric surgery (Fig. 3).
Fig. 3.
Changes of BMD and TBS before, 3 months and 1 year after bariatric surgery in women with different degrees of obesity. A: femoral neck BMD B total hip BMD C lumbar spine BMD D TBS Values. * p < 0.05, 3 months after surgery VS before surgery; ** p < 0.05, 1 year after surgery VS 3 months after surgery;#p < 0.05, 1 year after surgery VS before surgery.
Linear regression analysis of the relationships between the TBS and relevant variables 1 year after bariatric surgery (Fig. 4; Table 5)
Fig. 4.
Correlation between TBS and the above factors 1 year after surgery. A: Legs fat% B Trunk fat% C Total fat% D Android fat%.
Table 5.
Relationship between TBS and relevant variables 1 year after surgery.
| Variable | Correlation coefficient | p-value |
|---|---|---|
| BMI(kg/m2) | -0.107 | 0.547 |
| Femoral neck BMD (g/cm2) | 0.114 | 0.529 |
| Total hip BMD (g/cm2) | 0.338 | 0.063 |
| Lumbar spine BMD (g/cm2) | -0.188 | 0.558 |
| Total | ||
| BMC(kg) | 0.351 | 0.093 |
| FM(kg) | -0.055 | 0.793 |
| LM(kg) | 0.252 | 0.299 |
| fat% | -0.512 | 0.025* |
| Trunk | ||
| FM(kg) | -0.028 | 0.895 |
| LM(kg) | 0.244 | 0.314 |
| fat% | -0.503 | 0.028* |
| Android | ||
| FM(kg) | -0.028 | 0.893 |
| LM(kg) | 0.152 | 0.449 |
| fat% | -0.455 | 0.017* |
| VAT mass(g) | -0.388 | 0.100 |
| VAT volume(cm3) | -0.248 | 0.213 |
| Gynoid | ||
| FM(kg) | -0.078 | 0.710 |
| LM(kg) | 0.181 | 0.367 |
| fat% | -0.429 | 0.025* |
| Arms | ||
| FM(kg) | -0.131 | 0.532 |
| LM(kg) | 0.230 | 0.249 |
| fat% | -0.209 | 0.317 |
| Legs | ||
| FM(kg) | -0.089 | 0.674 |
| LM(kg) | 0.280 | 0.246 |
| fat% | -0.482 | 0.037* |
| FMI(kg/m2) | -0.098 | 0.640 |
| LMI(kg/m2) | 0.042 | 0.837 |
| aLMI(kg/m2) | 0.030 | 0.881 |
| T/A LMR | -0.027 | 0.893 |
| TFM/TLM | -0.384 | 0.064 |
| AFM/ALM | -0.368 | 0.077 |
| fat% trunk / fat%legs | 0.136 | 0.500 |
| A/G FMR | 0.023 | 0.913 |
* p < 0.05, there was a statistical difference.
One year after surgery, the TBS was negatively correlated with leg fat%, trunk fat%, total fat% android fat%, and no correlations were identified with other variables.
Discussion
Due to changes in people’s lifestyles and the extension of lifespans, the incidence and fatality rates of obesity and osteoporosis have increased annually, and these conditions have become two major social problems endangering human health. In fact, an important connection has been noted. Previous studies have shown that obesity is positively correlated with better bone metabolism and can reduce the risk of fracture19. However, recent studies have shown that the fracture risk of obese people has increased, and the fracture risk of obese people is site-specific and affected by age, sex, race and other factors20,21. A recent large prospective study in Norway revealed that the risk of hip fracture increased by 86% in women and 100% in men as waist circumference increased22. Therefore, the evaluation of bone health status, including bone mineral density and MA changes, after bariatric surgery can provide a basis for the clinical evaluation of the postoperative efficacy of bariatric surgery in patients with obesity and subsequent accurate follow-up treatment for this population. In our research center, DXA was used to evaluate the precision of measurements in 30 healthy volunteers. The results revealed that the precision (RMS-CV) values of the BMD (L1–4) and TBS (L1–4) were < 0.7% and 0.1%, respectively. The results indicated that the repeatability of BMD and TBS assessed using DXA was good.
Changes in BMD after bariatric surgery
The main determinants of bone strength are BMD and MA. Researchers have expressed different opinions on the changes in lumbar bone mineral density after weight loss. Most of the prospective reviews and meta-analyses23–26 evaluating BMD changes after bariatric surgery are limited by small sample sizes. In the first 12 months after bariatric surgery, a significant decrease in BMD was observed, with a femoral neck BMD of approximately 9–10% and a vertebral BMD of 3.6–8%24. Researchers have speculated that this reduction may be a normal adaptive change in bone mass, in which weight gradually becomes stable and the bone load gradually decreases after bariatric surgery25. BMD decreases after weight loss beyond the first year after bariatric surgery in very few cases27,28. In most cross-sectional and retrospective studies comparing patients who underwent bariatric surgery with controls, bone mineral density levels in the femoral neck, lumbar spine, and radius were similar to or greater after bariatric surgery than before surgery29. A study by Bredella30 revealed that the changes in bone mineral density after bariatric surgery were related to a decrease in lumbar BMD. Other relevant studies20,31,32 have shown that the BMD of the total hip and femoral neck decreased significantly after bariatric surgery compared with before surgery, and the earliest observed changes occur 6 months after bariatric surgery32. Some studies33 have shown that one year after bariatric surgery, the bone mineral density of patients’ lumbar spine, femoral neck and medullary joints all decreased, with the bone mineral density of the femoral neck decreasing most significantly.
In this study, the BMD (of the femoral neck, total hip, and lumbar spine) was within the normal range before and after bariatric surgery in both men and women, and the mean value was greater in men than in women. Bariatric surgery did not have significant adverse effects on BMD. In 41 patients who underwent three consecutive DXA examinations, time differences were observed in BMD changes; no significant changes were observed in the early period after weight loss (3 months after surgery), and the BMD decreased significantly 1 year after surgery (p < 0.05). The sites at which the BMD changed differed. The BMD decreased significantly in the proximal femur (femoral neck, whole hip) after bariatric surgery, but a significant change in the lumbar spine was not observed before or after surgery. Sex differences in the changes in BMD were noted. The BMD of the proximal femur (femoral neck and total hip) of male patients decreased significantly one year after surgery, whereas that of female patients did not change significantly. Changes in BMD are related to the degree of obesity. The BMD of men in the second- and third-degree obesity groups decreased significantly after bariatric surgery (p < 0.05).
Changes in the TBS before and after bariatric surgery
The impact of bariatric surgery on bone health has not been fully defined and has attracted increasing attention. Clinically, patients with normal BMD may also suffer fractures3, while patients with decreased BMD may also have excessively low bone mineral density due to the influence of factors such as the receptor lipid content, which indicates the importance of further evaluation of bone quality34. Precise methods for assessing MA have been developed, such as histomorphologic analysis, microcomputed tomography, transiliac ridge bone biopsy, high-resolution quantitative peripheral computed tomography35, magnetic resonance imaging, etc., but these tests are expensive and are not routinely used outside clinical trials. In contrast, the TBS may provide a simple and noninvasive method to assess MA after weight loss surgery. The ability of the TBS to predict fracture risk was partially independent of the DXA BMD, clinical risk factors, and fracture probability assessed using the Fracture Risk Assessment Tool (FRAX)36. Many studies have confirmed that the lumbar TBS can be used to evaluate not only lumbar vertebra bone quality but also femoral neck and hip bone quality and is a powerful tool for evaluating bone quality and predicting fracture risk5–8,37. In particular, for elderly patients with lumbar osteoarthritis, people with brittle fractures due to a BMD T value > -2.5, patients with T2DM, and patients with glucocorticoid-induced osteoporosis, the TBS is superior to the BMD for predicting fracture risk3,5–12,37,38. Several cross-sectional and prospective studies have shown associations between lumbar TBS and lumbar fractures, hip fractures, and other types of fractures in postmenopausal women39.
In this study, the TBS of both men and women before and after bariatric surgery were within the normal range, and the average TBS of men was greater than that of women. The TBS decreased slightly at 3 months and 1 year after bariatric surgery, the TBS of men and women at 1 year after bariatric surgery was the lowest, and bariatric surgery did not have significant adverse effects on the TBS. In 41 patients who underwent three consecutive DXA examinations, time differences in the TBS were detected, and no significant change was detected in the early stage after bariatric surgery (3 months after bariatric surgery); the TBS significantly decreased at 1 year after bariatric surgery (p < 0.05). No significant sex difference in TBS changes was observed, and the TBS decreased significantly in either men or women one year after bariatric surgery. The changes in the TBS were related to the degree of obesity and significantly decreased in the male third-degree obesity group, female second-degree obesity group and third-degree obesity group. Changes in the TBS are closely related to changes in BMD. The changes in the TBS differed from those in the BMD only in the female second-degree obesity group one year after bariatric surgery, and the changes in the TBS were the same as those in the BMD in the other obesity groups of different sexes. In one study, the TBS improved 1 year after bariatric surgery but decreased slightly 3 years after weight loss20. Therefore, further observations of whether the effect of MA changes again as the duration after bariatric surgery increases are necessary.
At present, the study population used to assess the TBS is still limited. Since most of the clinical research subjects satisfying the inclusion/exclusion criterions are postmenopausal women, few studies on men are available. Furthremore, as clinical research data are rather limited, research on assessing the TBS are still limited. A uniform threshold for distinguishing a normal from an abnormal TBS has not been identified6. The TBS has been reported to be lower in men than in women6, but this finding is different from previous histological and high-resolution quantitative computed tomography (QCT) findings showing that MA is better in males than in females35. In this study, MA was better in males than in females before and after bariatric surgery.
Correlations between the TBS and relevant variables after bariatric surgery
Evaluating the relationships between the TBS and related factors is important to better understand and apply the TBS. In this study, linear regression analysis of the TBS and related variables 1 year after bariatric surgery revealed that the TBS of patients 1 year after bariatric surgery was negatively correlated with leg fat%, trunk fat%, total fat%, and axial fat%, which was consistent with the conclusions of several previous studies20. The results showed that the improvement in fat distribution and the reduction in body fat after bariatric surgery resulted in an improvement in the TBS. In an analysis of changes in the TBS after bariatric surgery, premenopausal women and men undergoing bariatric surgery were randomly assigned to an intervention group that included strict supplementation with vitamin D, calcium, and protein, and muscle exercises compared with a nonintervention group in a controlled study. The TBS decreased in both groups and then remained stable in the intervention group (-3.4% vs. -10.5%)40. In most studies, the lumbar TBS was negatively correlated with BMI and FM41,42. Similar findings were described in Romagnoli’s study, which evaluated the TBS in overweight and obese men and reported that when a patient’s BMI was less than 35 kg/m2, body fat caused little image noise, increasing the accuracy of the TBS. However, some studies have reported that BMI and LM are more strongly positively correlated with BMD than FM27,43. In particular, the decrease in LM after bariatric surgery is a key factor contributing to the decrease in BMD, and no correlation between the TBS and total or regional LM was observed in this study.
The risk of fracture after bariatric surgery remains a controversial issue. In some studies, a two-fold increase in fracture risk1 has been observed after bariatric surgery. In other studies, an increased relative risk of fracture occurred only after malabsorption surgery44,45. However, a retrospective study using weight-matched controls conducted by Lahmohamed et al. included 2079 patients with an average follow-up of 2 years, and no changes in fracture risk were observed after bariatric surgery46. To date, there has been no available prospective studies that associates the risk of fracture with bariatric surgery.
Our study has several limitations. To interpret our results, we must consider that in an obese population, excessive soft tissue in the abdomen may reduce the TBS estimate, thus presurgical values can be altered by artifacts. Indeed, Agustina et al.17 reported a negative correlation between TBS values and greater body fat distribution in the trunk than in the legs. Similar findings were described in the Romagnoli study42, which evaluated the TBS in men with overweight/obesity and concluded that waist circumference, rather than BMI, should probably be considered when assessing the TBS. To eliminate the influence of soft tissue on the TBS measurement, the reduction in the TBS caused by thickening of the male abdominal soft tissue when the male and female BMIs are the same can be overcome by correcting the abdominal soft tissue of the subjects through corresponding software according to the BMI of the subjects so that there is no significant sex difference in the measurement results of the lumbar TBS47. In addition, current software can eliminate the effect of a subject’s BMI on the TBS of GE-LUNAR DXA, but it has not completely eliminated the effect of a subject’s BMI on Hologic DXA. Although the analysis software mentioned above can correct for the effect of this soft tissue thickness factor, some studies recommend that TBS be evaluated only in subjects with a BMI of 15 to 37 kg/m2. The assessment of people outside the BMI range also needs to be further studied. According to the study results of Mazzetti et al.48, the TBS evaluation results of DXA produced by Hologic and DXA produced by GE-LUNAR for the same population are different. The DXA results produced by Hologic revealed a negative correlation between the TBS and BMI (male r = -0.36, p = 0.000; female r = -0.33, p = 0.000), but the GE-LUNAR DXA results revealed that there was no significant correlation between the TBS and BMI. In addition, researchers have suggested that leptin and adiponectin may play a mediating role between surgery and bone mineral density changes, but these indicators were not recorded in our study; therefore, the influence of adipokines on changes in the TBS could not be analyzed. According to the above related studies on the measurement principle and clinical application range of the TBS, the TBS has adaptability and corresponding advantages as an evaluation index for clinical bone measurements. The use of a TBS in subjects with a BMI over 37 kg/m2 has not yet been validated. However, this is an intrinsic limitation of the technique, and the manufacturers are currently working on formulas for BMI correction that are not yet available. However, despite the technique limitations, TBS offers a noninvasive method to assess bone MA.
Conclusions
In our study of 41 patients that underwent DXA imaging before, 3 months after and 1 year after bariatric surgery, BMD (femoral neck, total hip, and lumbar spine) and TBS were within the normal ranges after bariatric surgery. The changes in the BMD and TBS before and after bariatric surgery differed with respect to time, degree of obesity, and sex. BMD and the TBS did not change significantly after bariatric surgery. A negative correlation was found between the TBS and fat percentage was observed 1 year after surgery, and the TBS improved with increasing fat distribution and decreasing body fat after weight loss.
DXA can be used to evaluate changes in body composition, BMD and MA in patients with obesity after bariatric surgery. The main determinants of bone strength are BMD and MA. An accurate assessment of the changes in bone strength after bariatric surgery is very important because it can greatly reduce the risk of fracture after bariatric surgery and ensure the quality of life of patients. However, whether the effect on bone strength changes persist after bariatric surgery needs further validated.
Author contributions
Huimin You and Jingjie Shang wrote the main manuscript text and Wenjun He and Zhenjun Huang prepared figures and tables. Jian Gong, Hao Xu and Chunping Zeng reviewed and guided article. All authors reviewed the manuscript.
Funding
Guangdong Provincial Bureau of Traditional Chinese Medicine, Project Number: 20222129
Data availability
This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the noncommercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited. See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
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The first two authors participated equally in this article and would qualify for first authorship.
These authors contributed equally: Hao Xu, Jian Gong.
Contributor Information
Hao Xu, Email: txh@jnu.edu.cn.
Jian Gong, Email: gongjian2021@163.com.
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Data Availability Statement
This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the noncommercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited. See: https://creativecommons.org/licenses/by-nc-nd/4.0/.