Abstract
Background
Both general and central obesity have been linked to vertebral fractures; however, their specific effects on vertebral fractures have not been directly compared. This study aimed to investigate the associations between measures of general and central obesity and vertebral fractures.
Methods
This cross-sectional study of 1,011 postmenopausal women used dual-energy X-ray absorptiometry to measure bone density and body composition. Bone quality was assessed using the trabecular bone score. General obesity was evaluated using body mass index and body fat percentage, whereas central obesity was measured using waist circumference, waist-hip ratio, and android-gynoid ratio.
Vertebral fractures were determined by retrospectively reviewing medical records, and only fractures confirmed by radiological reports were included.
Results
Obesity indices, including body mass index, body fat percentage, waist circumference, and android-gynoid ratio, were positively associated with bone density but negatively associated with trabecular bone score. General obesity, based on body fat percentage, was associated with vertebral fractures, whereas general obesity measured using body mass index was not. Central obesity assessed using waist circumference, waist-hip ratio, and android-gynoid ratio, was associated with vertebral fractures. Furthermore, among the different combinations of general and central obesity, central obesity measured by waist circumference and waist-hip ratio was still associated with vertebral fractures, irrespective of general obesity.
Conclusions
Central obesity was more strongly associated with vertebral fractures than general obesity in postmenopausal women. Therefore, developing and implementing measures to prevent central obesity are recommended.
Keywords: Android-gynoid ratio, Central obesity, General obesity, Vertebral fractures, Waist circumference, Waist-hip ratio
Introduction
Obesity is a major global public health concern. Various measures are available for diagnosing obesity. For example, general obesity can be evaluated using body mass index (BMI) or total body fat percentage, whereas central obesity could be identified using waist circumference, waist-hip ratio, or android-gynoid ratio [1]. Fat distribution may have different effects on bone mass [2]; similarly, general and central obesity may have different impacts on bone strength. However, the differential effects have not been explored in the literature.
Previous studies have reported the association of general or central obesity indices with bone mineral density (BMD). Chen et al. showed that general obesity, as assessed using BMI and body fat percentage, was associated with low bone mass in men rather than in women [3]. Kim et al. reported that general obesity based on body fat percentage and central obesity measured using waist circumference were positively associated with BMD in men ≥ 50 years and in premenopausal and postmenopausal women [4]. Yoo et al. showed that general obesity, defined as body fat percentage was associated with BMD in premenopausal women but not in men or postmenopausal women [5]. Therefore, the results regarding the association between general or central obesity and BMD remain inconclusive.
Recent studies have demonstrated that the association between obesity indices and fractures varies according to the fracture site. For instance, general obesity based on BMI was associated with proximal humeral [6, 7] and vertebral fractures [8], whereas it was protective against hip [6, 7], pelvic [7, 8], and distal forearm fractures [6]. Central obesity, as measured using the waist circumference, was associated with an increased risk of vertebral and hip fractures [9, 10]. However, these studies did not compare the effects of general and central obesity indices on fractures. Therefore, because general and central obesity indices were both associated with vertebral fractures, we aimed to investigate and compare the association of general and central obesity indices with bone strength, as well as their influence on vertebral fractures.
Methods
Participants
This cross-sectional study was conducted between January 2019 and September 2023. Participants were randomly recruited from individuals who underwent dual-energy X-ray absorptiometry (DXA) at our hospital. The inclusion criteria were postmenopausal women aged 40 to 92 years with a BMI of 15–37 kg/m2. The exclusion criterion was the inability to perform anthropometric measurements or body composition analysis in participants, because of physical or cognitive disability. Finally, 1,011 participants were enrolled in this study, all of whom provided written informed consent. This study was approved by the institutional review board of Cheng Hsin General Hospital (IRB no. (660)107 A-32).
Anthropometric measurements
Participants were requested to change into light clothing when their weight and height were measured. Waist circumference was measured at an approximate midpoint between the top of the iliac crest and the lower margin of the last palpable rib, while hip circumference was evaluated at the widest portion of the buttocks [11]. The waist and hip circumferences were used to calculate the waist-hip ratio.
Bone mineral density and bone quality
The BMD of the lumbar spine (L1–L4) was measured using a DXA scanner (Horizon W; Hologic Inc., Bedford, MA, USA). In accordance with the 2023 official positions of the International Society for Clinical Densitometry, fractured vertebrae and those showing a T-score difference of more than 1.0 compared to adjacent vertebrae were excluded from the spinal BMD analysis [12]. The bone quality was evaluated using the trabecular bone score (TBS) recommended by the International Society for Clinical Densitometry [13]. The TBS was calculated using iNsight software (version 3.0.2.0, Medimaps, Geneva, Switzerland) based on the DXA image [14]. The coefficient of variation was 0.94% for the lumbar spine BMD and 2.00% for the TBS.
Body composition analysis
Body fat percentage, appendicular lean mass (ALM), and android-gynoid ratio were assessed using whole-body DXA scanner (Horizon W; Hologic Inc., Bedford, MA, USA). The height of the android region of interest (ROI) was 20% of the distance from the pelvic horizontal line to the neck line. The height of the gynoid ROI was twice that of the android ROI and the upper border was below the pelvic horizontal line by 1.5 times the height of the android ROI [1]. The android-gynoid ratio was measured by dividing the android fat mass by the gynoid fat mass.
Definitions of general and central obesity
General obesity was evaluated using BMI and body fat percentage, whereas central obesity was identified using waist circumference, waist-hip ratio, and android-gynoid ratio. BMI ≥ 27 kg/m² and waist circumference ≥ 80 cm are used to define general and central obesity, respectively, by the Health Promotion Administration of the Taiwanese government [15]. For central obesity using the waist-hip ratio, a cutoff ratio of ≥ 0.85 was recommended by the World Health Organization [11]. However, no established cutoff values for body fat percentage or the android-gynoid ratio were available in our country. Therefore, we defined the cutoff values in this study based on the highest tertiles of these measures. Accordingly, a body fat percentage of ≥ 45.4% and an android-gynoid ratio of ≥ 1.05 were considered indicative of general and central obesity, respectively.
Assessment of vertebral fractures
Prevalent vertebral fractures were assessed by retrospectively reviewing the hospital medical records of all participants. Only fractures confirmed by radiological reports were included in the analysis.
Covariates
Covariates included age; dairy product intake more than three times per week (yes vs. no); regular physical activity for at least 30 min per day on more than three days per week (yes vs. no); and use of medications affecting bone strength, including bisphosphonates, parathyroid hormone, estrogen, and corticosteroids (yes vs. no).
Statistical analysis
Multiple linear regression analysis was used to estimate the associations of various obesity indices with BMD or TBS. Multivariable logistic regression analysis was used to evaluate the association of general and central obesity with vertebral fractures. Participants were categorized into four composite groups based on the presence or absence of general and central obesity. Multivariable logistic regression analysis was conducted to evaluate the association between these obesity classifications and vertebral fractures. The Shapiro-Wilk test was used to assess the normality of unstandardized residuals. A two-sided p < 0.05 was considered statistically significant. Analyses were performed using SPSS for Windows, version 19.0 (IBM Corp., Armonk, NY, USA).
Results
Table 1 shows the demographic characteristics of the participants. Participants aged 60 years and older made up 71.2% of the total. The mean age, BMI, waist circumference, and waist-hip ratio were 64.2 years, 23.9 kg/m2, 80.5 cm, and 0.86, respectively. According to the body composition analysis, the mean body fat percentage, android-gynoid ratio, and ALM were 43.2%, 1.0, and 12.3 kg, respectively. The mean lumbar spine BMD was 0.817 g/cm2 and the mean TBS was 1.276. The prevalence of general obesity was 19.5% based on BMI and 34.3% based on body fat percentage. In contrast, the prevalence of central obesity measured by waist circumference, waist-hip ratio, and android-gynoid ratio were 52.0%, 49.5%, and 36.7%, respectively.
Table 1.
Characteristics of the participants (n = 1,011)
| Age (years, mean ± SD) | 64.2 ± 8.8 |
|---|---|
| Anthropometric measurements (mean ± SD) | |
| Weight (kg) | 57.9 ± 9.5 |
| Height (cm) | 155.7 ± 5.8 |
| Body mass index (kg/m2) | 23.9 ± 3.8 |
| Waist circumference (cm) | 80.5 ± 9.5 |
| Hip circumference (cm) | 94.2 ± 8.3 |
| Waist-hip ratio | 0.86 ± 0.08 |
| Body composition analysis (mean ± SD) | |
| Body fat percentage (%) | 43.2 ± 5.0 |
| Android-gynoid ratio | 1.0 ± 0.1 |
| Appendicular lean mass (kg) | 12.3 ± 1.9 |
| Lifestyle factors, n (%) | |
| Physical activity | 327 (32.3) |
| Dairy product intake | 384 (38.0) |
| Medications | 170 (16.8) |
| Bone mineral density (g/cm2, mean ± SD) | |
| Lumbar spine | 0.817 ± 0.15 |
| Trabecular bone score (mean ± SD) | 1.276 ± 0.09 |
| General obesity, n (%) | |
| Based on BMI | 197 (19.5) |
| Based on body fat percentage | 347 (34.3) |
| Central obesity, n (%) | |
| Based on waist circumference | 526 (52.0) |
| Based on waist-hip ratio | 500 (49.5) |
| Based on android-gynoid ratio | 371 (36.7) |
The associations between different obesity indices and bone strength were presented in Table 2. The correlation coefficients were 0.284, 0.131, 0.169, 0.020, and 0.133 for BMI, body fat percentage, waist circumference, waist-hip ratio, and android-gynoid ratio, respectively. All obesity indices (except for the waist-hip ratio), including BMI, body fat percentage, waist circumference, and android-gynoid ratio showed a positive association with bone density. The largest correlation coefficient was observed for BMI compared with the other obesity indices. The value of R2 represents the exploratory power of the model. The R2 values in the models were 0.147, 0.116, 0.115, 0.097, and 0.115 for BMI, body fat percentage, waist circumference, waist-hip ratio, and android-gynoid ratio, respectively. The R2 value was higher for BMI than for other obesity indices. Additionally, ALM was positively associated with BMD, whereas physical activity was not. However, all obesity indices were negatively associated with the TBS, and the largest correlation coefficient of 0.178 was observed for waist circumference. The R2 values were similar, ranging between 0.278 and 0.284, in the TBS models. We further investigated the association between the obesity indices and vertebral fractures (Table 3). General obesity based on body fat percentage was associated with vertebral fractures but not with BMI. Central obesity, assessed using waist circumference, waist-hip ratio, and android-gynoid ratio, was associated with vertebral fractures. Additionally, ALM and physical activity were not associated with vertebral fractures.
Table 2.
Multiple regression standardized coefficients (β) of obesity indices for spinal bone mineral density and trabecular bone score
| Spinal bone mineral density | Trabecular bone score | |
|---|---|---|
| Model 1 | ||
| Body mass index | 0.284* | −0.149* |
| R2 | 0.147 | 0.279 |
| Model 2 | ||
| Body fat percentage | 0.131* | −0.113* |
| R2 | 0.116 | 0.278 |
| Model 3 | ||
| Waist circumference | 0.169* | −0.178* |
| R2 | 0.115 | 0.282 |
| Model 4 | ||
| Waist-hip ratio | 0.020 | −0.143* |
| R2 | 0.097 | 0.282 |
| Model 5 | ||
| Android-gynoid ratio | 0.133* | −0.140* |
| R2 | 0.115 | 0.284 |
All regression models were adjusted for age, appendicular lean mass, medications, physical activity, and dairy product intake
*p < 0.05
Table 3.
Multivariable logistic regression for vertebral fractures according to different diagnostic methods for obesity
| Odds ratio | 95% Confidence interval | |
|---|---|---|
| Model 1: obesity assessed by body mass index | ||
| Yes vs. No | 1.06 | 0.62–1.80 |
| Model 2: obesity assessed by body fat percentage | ||
| Yes vs. No | 1.50 | 1.03–2.16 |
| Model 3: obesity assessed by waist circumference | ||
| Yes vs. No | 2.19 | 1.47–3.27 |
| Model 4: obesity assessed by waist-hip ratio | ||
| Yes vs. No | 1.90 | 1.30–2.79 |
| Model 5: obesity assessed by android-gynoid ratio | ||
| Yes vs. No | 1.51 | 1.04–2.18 |
All regression models were adjusted for age, spinal bone mineral density, trabecular bone score, appendicular lean mass, medications, physical activity, and dairy product intake
Participants were classified into four groups based on their general and central obesity statuses. As obesity based on BMI was not associated with vertebral fractures in this study, general obesity measured using body fat percentage was categorized into composite groups. Using the group without general and central obesity as a reference, participants with both general and central obesity showed the highest likelihood of vertebral fractures (Table 4). Furthermore, participants who only had general obesity were not associated with vertebral fractures. Most importantly, central obesity, assessed by waist circumference and waist-hip ratio, irrespective of the presence of general obesity, was significantly associated with vertebral fractures. The Shapiro-Wilk test was used to confirm the normal distribution of unstandardized residuals in all models (p > 0.05).
Table 4.
Multivariable logistic regression for vertebral fractures according to different combinations of general and central obesity
| Odds ratio | 95% Confidence interval | ||
|---|---|---|---|
| Model 1 | |||
| Body fat percentage (%) | Waist circumference (cm) | ||
| < 45.4 | < 80 | 1 | |
| ≥ 45.4 | < 80 | 1.02 | 0.43–2.45 |
| < 45.4 | ≥ 80 | 2.04 | 1.25–3.32 |
| ≥ 45.4 | ≥ 80 | 2.36 | 1.47–3.79 |
| Model 2 | |||
| Body fat percentage (%) | Waist-hip ratio | ||
| < 45.4 | < 0.85 | 1 | |
| ≥ 45.4 | < 0.85 | 1.07 | 0.55–2.07 |
| < 45.4 | ≥ 0.85 | 1.61 | 1.01–2.61 |
| ≥ 45.4 | ≥ 0.85 | 2.48 | 1.50–4.11 |
| Model 3 | |||
| Body fat percentage (%) | Android-gynoid ratio | ||
| < 45.4 | < 1.05 | 1 | |
| ≥ 45.4 | < 1.05 | 1.51 | 0.90–2.52 |
| < 45.4 | ≥ 1.05 | 1.51 | 0.93–2.46 |
| ≥ 45.4 | ≥ 1.05 | 2.05 | 1.24–3.40 |
All regression models were adjusted for age, spinal bone mineral density, trabecular bone score, appendicular lean mass, medications, physical activity, and dairy product intake
Discussion
In this study, we investigated the association of general and central obesity with bone strength and compared their association with vertebral fractures. We found that obesity indices were positively associated with bone density, but negatively associated with TBS. Among the different combinations of general and central obesity, general obesity measured using body fat percentage without central obesity was not associated with vertebral fractures. Furthermore, central obesity, assessed by waist circumference and waist-hip ratio, was still associated with vertebral fractures, irrespective of general obesity. Therefore, central obesity was more strongly associated with vertebral fractures than general obesity.
Previous studies have shown that general and central obesity indices were positively associated with spinal BMD [4] and that the correlation coefficient of fat mass was higher than that of other obesity indices, similar to our results. Additionally, we found that ALM was positively associated with BMD and that ALM contributed to BMD in both men and women [4, 16]. Therefore, maintaining ALM is important for bone health. The National Institutes of Health defines bone strength as the integration of bone density and quality [17]. TBS is a commonly used non-invasive method for evaluating bone quality. Our results demonstrated that general and central obesity indices were negatively associated with the TBS. In the literature, increased soft tissue over the region of interest (lumbar spine) resulted in differences in the spinal BMD and TBS. Although BMD was affected, it was unlikely to lead to a clinical problem because the change did not exceed the least significant change [18]. In contrast, increased soft tissue thickness resulted in a lower TBS value [18, 19]. The correlation with waist circumference was therefore stronger in our study, which was consistent with the results of a previous study [20]. Shevroja et al. developed a soft tissue-adjusting technique for computing the TBS, and showed that obesity indices were positively correlated with the TBS, indicating better bone quality [19]. However, accumulating evidence supports the association between obesity and compromised bone quality [21]. Cohen et al. also reported that central obesity was associated with inferior bone quality, as measured by trans-iliac crest bone biopsy [22]. Further studies are required to determine which TBS algorithm is the most suitable for evaluating obesity.
Accumulating evidence has challenged the protective effects of obesity against fractures, and the association between obesity and fractures appears to be site-dependent. However, studies investigating the association between general obesity and vertebral fractures have yielded conflicting results. Prieto-Alhambra et al. reported that general obesity, measured using BMI, was not associated with vertebral fractures [7], whereas Liu et al. found that general obesity, assessed using BMI, was associated with an increased risk of vertebral fractures [8]. Additionally, different diagnostic measures for assessing obesity may affect its association with fractures. Gandham et al. reported that general obesity, based on body fat percentage, was associated with fractures, whereas obesity measured using BMI was not; [23] this finding was consistent with our results.
Several studies have investigated the association between general obesity and fractures. However, few have examined the association between central obesity and vertebral fractures. In the Nurses’ Health Study, women aged 30–55 years with central obesity (measured using waist circumference ≥ 108 cm) showed an increased risk of vertebral fractures [24]. Another prospective study in the South Korean population aged ≥ 40 years reported that central obesity (assessed using waist circumference: men ≥ 90 cm and women ≥ 85 cm) was positively associated with the risk of vertebral fracture [9]. Similarly, in a prospective study with subjects aged > 50 years in China, central obesity (based on waist circumference: men > 90 cm, women > 80 cm; waist-hip ratio: men > 0.9, women > 0.85) was associated with a higher risk of subsequent vertebral fractures [25]. In our study, postmenopausal women with both general and central obesity showed the highest likelihood of vertebral fractures and central obesity (measured using waist circumference ≥ 80 cm and waist-hip ratio ≥ 0.85) showed a stronger association with vertebral fractures than general obesity.
Several studies have proposed explanations for the association between central obesity and fractures. First, individuals with obesity, particularly central obesity, may have a higher risk of falling [26]. Second, central obesity may place a higher burden on the spine and increase impact force despite the protective effect of soft tissue pads [27, 28]. Third, visceral fat adversely affected bone quality by altering bone-regulating hormone levels, oxidative stress, and inflammation [21, 22]. Fourth, the distribution of body fat, especially in central obesity, can potentially have different effects on the bone [2], and compared to general obesity, central obesity may increase the risk of vertebral fracture. The relationship between obesity and fractures is a complex and multifaceted issue, and further studies are required to clarify the underlying mechanisms.
This study had the strength in using various common diagnostic measures for assessing general and central obesity that can be applied in clinical practice. To the best of our knowledge, this study is the first to compare the association of different combinations of general and central obesity indices with vertebral fractures. However, our study had several limitations. First, this was a cross-sectional study; therefore, the causal inferences between obesity and vertebral fractures could not be made. Second, the participants in our study were limited to the Asian population, and obesity was defined by Asian criteria, which may have affected the generalizability of our results. Third, the association between obesity and fractures is site-specific. In our study, we focused only on vertebral fractures, and further investigation of different fracture sites is required to reveal additional relationships. Fourth, in this study, vertebral compression fractures were confirmed using radiological reports. While X-rays are not sensitive enough to detect occult fractures, they are the most accessible tool for assessing compression fractures, especially when compared to CT or MRI, which are less readily available due to higher costs and limited accessibility. Fifth, our study only included postmenopausal women. Therefore, our results may not apply to men or premenopausal women. Further studies involving diverse populations are needed to confirm our findings.
Conclusions
We investigated the association of different diagnostic measures for assessing obesity with vertebral fractures in postmenopausal women and found that central obesity was more strongly associated with vertebral fractures than general obesity. Therefore, developing and implementing measures to prevent central obesity are recommended; however, further longitudinal studies may be required to demonstrate whether vertebral fractures can be prevented by managing central obesity.
Acknowledgements
Not applicable.
Abbreviations
- ALM
Appendicular lean mass
- BMI
Body mass index
- DXA
Dual-energy X-ray absorptiometry
- BMD
Bone mineral density
- TBS
Trabecular bone score
Authors’ contributions
Yen-Huai Lin and Michael Mu Huo Teng initiated the study, and all authors contributed to its design. Yen-Huai Lin and Michael Mu Huo Teng managed the data collection, performed the data analysis, and wrote the first draft of the manuscript. Yen-Huai Lin and Michael Mu Huo Teng are collectively responsible for interpreting the results and critically reviewed subsequent drafts of the manuscript. All authors read and approved the final manuscript.
Funding
This work was supported by a grant (CHGH114-113-N23) from the Cheng Hsin General Hospital, Taipei, Taiwan.
Data availability
The data that support the findings of this study are available from the authors but restrictions apply to the availability of these data, which were used under license from Cheng Hsin General Hospital for the current study, and so are not publicly available. Data are, however, available from the authors upon reasonable request and with permission from the institutional review board of Cheng Hsin General Hospital.
Declarations
Ethics approval and consent to participate
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the institutional review board of Cheng Hsin General Hospital (IRB no. (660)107A-32).
Informed consent was obtained from all the participants included in the study.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the authors but restrictions apply to the availability of these data, which were used under license from Cheng Hsin General Hospital for the current study, and so are not publicly available. Data are, however, available from the authors upon reasonable request and with permission from the institutional review board of Cheng Hsin General Hospital.