Abstract
Although obesity was once considered protective against osteoporosis, various factors influence the relationship between fat and bone mineral density (BMD). To establish the importance of healthy body composition in decelerating declines in BMD, we conducted a study to compare the association between body fat composition and BMD in Korean adults. Using data collected from the Kangbuk Samsung Health Study from 2012 to 2019, this cohort study compared the incidence of decreased BMD among the following four groups: normal BMI and normal adiposity (NBMI-NA), normal BMI and high adiposity (NBMI-HA), overweight, and obesity. Decreased BMD was defined as a Z-score ≤ − 2.0 in premenopausal women and men < 50 years of age or a T-score < − 1.0 in postmenopausal women and men ≥ 50 years of age. Individuals who were diagnosed with osteoporosis or compression fracture after their second visit were categorized as having decreased BMD. The incidence rate of decreased BMD in the NBMI-NA group was 3.37, and that in the NBMI-HA group was 4.81, which was the highest among all groups. After adjusting for confounding factors, NBMI-HA led to a significantly greater risk of decreased BMD compared to NBMI-NA (HR 1.47; 95% CI 1.09–1.99). Even with a normal BMI, a high BFP was associated with an increased risk of decreased BMD. Therefore, healthy body composition management, not simply BMI, is important in preventing decreased BMD.
Similar content being viewed by others
Introduction
The prevalence of osteoporosis is increasing among both women and men, and it is associated with elevated risks of all-cause mortality, mortality from cardiovascular disease, respiratory disease, and cancer1,2. Until the age of 30 years, through the remodeling process, reabsorbed bone is replaced with an equal amount of new bone tissue. However, after the age of 30–45 years, an imbalance in bone tissue absorption and formation occurs, and the rate of absorption of bone tissue eventually exceeds the rate of formation3,4. Many drugs have been approved for the treatment of osteoporosis to slow the loss of bone density. However, no drug can “cure” osteoporosis. Therefore, an essential goal in reducing the mortality risk is to decelerate the decline in bone mineral density (BMD) prior to the onset of osteoporosis.
Following the start of the coronavirus disease 2019 pandemic, people’s weights increased due to reduced physical activity, overeating, and increased stress5. As a result, there has been an increase in the number of individuals attempting to manage their health, with most simply focusing on body mass index (BMI)6. In the past, obesity was traditionally considered a protective factor against osteoporosis, resulting in the so-called “obesity paradox7,8.” However, recent studies have shown that both multiple factors affect the relationship between bone and adipose tissue, and that fat adversely affects bone tissue9,10. Adipose tissue acts as an endocrine organ that promotes bone resorption, inhibits bone formation, and provides mechanical loading to protect against bone loss11,12,13. In previous cross-sectional studies, when weight was corrected to exclude the effects of the physical load of fat, a negative correlation was found between adipose tissue and bone density, and the correlation between fat and bone density varied according to age and sex14,15,16. However, to our knowledge, no cohort study has definitively established the association between high body fat percentage and decreased BMD in individuals, including menopausal women, men or in premenopausal women.
Thus, we conducted a retrospective cohort study to investigate the relationship between body fat and decreased BMD in Korean adults after adjusting for the effects of physical loading on fat. Our study sought to demonstrate that managing body composition for overall health, rather than relying solely on BMI-based health management strategies, is crucial for preventing declines in BMD.
Method
Study subjects
A retrospective cohort study was conducted on men and women aged ≥ 18 years who registered in the cohort study database of Kangbuk Samsung Hospital Total Healthcare Center in Seoul and Suwon, Republic of Korea, from January 1, 2012, to December 31, 2019. The study subjects underwent comprehensive health screening examinations at Kangbuk Samsung Hospital Total Healthcare Center. According to the industrial Safety and Health Law in Republic of Korea, all employees of large companies are required to undergo annual or biennial health examinations. Among the study participants, more than 80% were either employees of companies or their family members17. Participants who underwent bone density measurement ≥ 2 times by dual-energy X-ray absorptiometry (DXA) bone-density scanning were included in this study. Participants were excluded if they had osteoporosis at the time of their first visit or if they satisfied the World Health Organization (WHO) criteria for osteopenia or osteoporosis based on bone density measurements18. Patients were also excluded if information about their demographic characteristics or body measurements was missing or if their body weight was too low (defined by BMI < 18.5 kg/m2).
Anthropometric and biochemical measurements
Based on the Kangbuk Samsung Health Study, the demographic characteristics, body measurements, and biochemical tests of the study participants were investigated. Body fat mass (kg) was measured through bioelectric impedance analysis (Inbody720; Biospace, Seoul, Republic of Korea), and the body fat percentage (BFP) was estimated by dividing body fat mass by body weight19. Postmenopausal women were defined as women who responded “yes” to experiencing “no menstruation for > 1 year” in the questionnaire.
Four categories of BMI and BFP
Participants were classified into four groups according to BMI and BFP values. To investigate the association between body fat and decreased BMD when the BMI was normal, participants with normal BMI were also classified based on a 30% BFP cutoff20. Additionally, to confirm the association between obesity and decreased BMD, study participants with high BMIs were divided into overweight and obesity groups. The WHO Asia–Pacific Centre and the Korean Society of Obesity define patients with a BMI of 23–24.9 kg/m2 as overweight and those with a BMI ≥ 25 kg/m2 as obese. The diagnostic criteria used in this study for assigning participants into the overweight and obesity groups by BMI were based on these criteria21,22, and the final four study groups were as follows: (1) normal BMI and normal adiposity (NBMI-NA), BMI of 18.5–22.9 kg/m2 and BFP < 30%; (2) normal BMI and high adiposity (NBMI-HA), BMI of 18.5–22.9 kg/m2 and BFP ≥ 30%; (3) overweight, BMI of 23–24.9 kg/m2; and (4) obesity: BMI ≥ 25 kg/m2.
Measurement of BMD
BMD was measured by DXA (Prodigy [GE Healthcare, Madison, WI, USA] or HOLOGIC QDR 4500W [Hologic Inc., Bedford, MA, USA]). In premenopausal women and men < 50 years of age, a Z-score was obtained by comparing each patient’s BMD with the average BMD of the same age group. In postmenopausal women and men ≥ 50 years of age, the T-score was obtained by comparing each patient’s BMD with the BMD of the young adult group.
Definition of decreased BMD
A decreased BMD was recorded when ≥ 1 of the following three conditions was satisfied: (1) a total lumbar or femur neck or total femur Z-score ≤ − 2.0 in premenopausal women or men < 50 years of age during the second and subsequent BMD measurement through DXA within the study period; (2) a total lumbar or femur neck or total femur T-score < − 1.0 in postmenopausal women or men > 50 years of age during the second and subsequent BMD measurement through DXA, based on the WHO criteria of osteopenia and osteoporosis18; and (3) diagnosed with osteoporosis, had taken medication for osteoporosis, or had a compression fracture as recorded during the second and subsequent questionnaires within the study period.
Statistical analysis
Statistical analysis was conducted according to the four categories of BMI and BFP. Continuous variables were described with mean and standard deviation values, and mean comparisons among the four groups were analyzed by one-way analysis of variance. If the distribution was not normal, the median (interquartile range) value was tested with the Kruskal–Wallis H test. Categorical variables were described by frequency and ratio, and Pearson’s chi-square test was used to test the difference in ratios between the four groups. To confirm the incidence of decreased BMD in each group, the total number of person-years was calculated by summing the observation periods of the study subjects (Table 2). The observation period was defined as the time from occurrence of decreased BMD relative to the first DXA measurement. The incidence rate per 1000 person-years was calculated by dividing the number of people with decreased bone density by the total number of person-years and multiplying by 1000. Hazard ratios (HRs) and 95% confidence intervals (CIs) for decreased BMD in the four groups were obtained using a Cox proportional hazards model with adjustments for confounders (Table 3). Statistical analyses were performed using STATA version 17.1 (StataCorp LLC, College Station, TX, USA).
Ethical approval
The present study did not include any animal studies. All procedures involved in this study of human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was conducted with approval from the Institutional Review Board (IRB) of Kangbuk Samsung Hospital (IRB no. 2022-10-055), which waived the requirement for informed consent as pre-existing de-identified data obtained from the Kangbuk Samsung Cohort Study was used for this study.
Results
Comparison of baseline characteristics
There were 3904 eligible participants for this study, including 3521 women and 383 men (Fig. 1). As shown in Table 1, the average age of the NBMI-NA and NBMI-HA groups was approximately 46.5 years, the average age of the overweight group was 49.4 years, and the average age of the obese group was 50.1 years. The average BMIs were 20.6 kg/m2 in the NBMI-NA group, 21.6 kg/m2 in the NBMI-HA group, 23.89 kg/m2 in the overweight group, and 27.45 kg/m2 in the obesity group. Notably, the mean BFP values of the NBMI-HA and overweight groups were similar (25.24% in the NBMI-NA group, 32.89% in the NBMI-HA group, 32.04% in the overweight group, and 36.28% in the obesity group). eTable 1 in the Supplementary section lists the characteristics of female participants, which were similar to those of all study participants.
Incidence of decreased BMD
Table 2 lists the incidence of decreased BMD in all study participants and female participants only. Regardless of sex, the total number of person-years of all participants was approximately 9527, and the median follow-up period was 2.03 years. During the observation period of a total of 9527 person-years, 336 people presented with reductions in BMD, and the incidence rate per 1000 person-years was 3.53. When comparing the incidence per 1000 person-years of decreased BMD across the four groups, the incidence rate in the NBMI-NA group was 3.37 and that in the NBMI-HA group was 4.81, which was the highest among all groups. When looking at the incidence of the decrease in bone density in female participants only, during the observation period of a total of 8322 person-years, decreased BMD was observed in 305 women, and the incidence rate per 1000 person-years was 3.66. In female participants, the incidence rate of the NBMI-NA group was 3.28 and that of the NBMI-HA group was 4.81, which was also the highest among all groups, just like among all study participants.
Table 3 shows the risk ratio of decreased BMD incidence for the NBMI-HA, overweight, and obesity groups in comparison to the incidence in the NBMI-NA group. For model 1, we adjusted for age and sex in males and additionally adjusted for menopausal status in female participants. In model 2, we additionally adjusted for BMI to adjust for the effects of physical load. In model 3, we adjusted for a history of rheumatoid arthritis, oral steroid usage, smoking, drinking, and physical activity23. Among all study participants, the NBMI-HA group showed a significantly greater risk of decreased BMD compared to the NBMI-NA group (in model 2: HR 1.43; 95% CI 1.07–1.93; in model 3: HR 1.47; 95% CI 1.09–1.99). The risk ratio of the overweight and obesity groups was greater than that of the NBMI-NA group (although not statistically significant) in model 2 and model 3. In only female participants, the NBMI-HA group showed a significantly higher risk of decreased BMD compared to the NBMI-NA group, which was in accordance with that of all study participants (in model 2: HR 1.52; 95% CI 1.11–2.07; in model 3: HR 1.56; 95% CI 1.14–2.13). In models 2 and 3, the obesity group showed a significantly higher risk of decreased BMD compared to the NBMI-NA group when considering only female participants.
Discussion
To the best of our knowledge, this is the first retrospective cohort study confirming the association between body fat and decreased BMD in Korean adults, including not only menopausal women, but also men and premenopausal women. In this cohort study, the incidence of decreased BMD was highest in the NBMI-HA group, with greater risk of decreased BMD compared to in the NBMI-NA group, regardless of the adjustments made. This suggests that, even if a person’s BMI is normal, the risk of decreased BMD increases if the BFP is high (BFP ≥ 30%).
Our results reinforce the findings from a Korean population study that showed a negative correlation between fat mass and BMD in women16. Moreover, previous studies have demonstrated that fat mass has a negative effect on bone mass in contrast with the positive effect of weight-bearing itself, and this aligns with the findings of this cohort study14,15. Therefore, we suggest that a personalized approach considering body fat is necessary for confirming bone health.
In a previous cross-sectional study using data from the Korea National Health and Nutrition Examination Survey from 2008 to 2011, fat mass positively affected the BMD of women and older men with normal BMIs24, which contradicts the results of this cohort study. However, our cohort study has the following strengths compared to the cross-sectional study. First, unlike the cross-sectional study that did not adjust for confounding factors, such as BMI, rheumatoid arthritis, and steroid use, this cohort study included these variables. Second, by confirming a positive correlation between BFP and decreased BMD, including in younger adults (premenopausal women and men < 50 years of age), this cohort study highlights the need for a healthy body composition management for bone health from a young age. With a previous study showing how body fat distribution plays an important role in determining bone density in young adults25, future cohort studies that consider body fat distribution will also be necessary.
The “obesity paradox” has been a source of confusion in metabolic studies7,8, but recent studies have shown that there are various factors affecting both fat and bone tissue, and the connection between them is not clear9,10,11,12,13. There is a variety of factors involved in the association between adipose tissue and bone tissue, including mechanical factors, metabolic factors, and hormones9. Mechanical association would be best explained by the increased physical loading due to adipose tissue26. However, physical loading alone is not sufficient to fully explain the interaction between adipose tissue and bone density27. Various hormones and cytokines are known to influence the interaction between adipose tissue and bone tissue. Aromatase, which synthesizes the estrogen that promotes bone formation and reduces bone resorption, is secreted not only in the gonads, but also in adipose tissue28. Although adipose tissue is thought to contribute to bone health through this mechanism, there are other factors involved as well. Leptin, which is mainly secreted from adipocytes, has been reported to have both positive29 and negative effects30,31 on bone formation, making it controversial. Adiposity is associated with the increase in inflammatory factors like C-reactive protein, tumor necrosis factor–α, and interleukin-6, which inhibit adiponectin that increases bone density32. Additionally, tumor necrosis factor–α and interleukin-6 promote osteoclastic resorption33,34. Other factors, such as vitamin D level and differences in adipose tissue distribution (visceral fat, subcutaneous fat) are involved in the association between fat and bone tissue, but the impact of these factors is still controversial35,36. Although it was difficult to confirm the effects of these various factors in this cohort study, this study still provided evidence that body fat and bone health are negatively correlated.
This study has several limitations. First, there are several factors that can affect the measurements obtained from a bioelectric impedance analysis (Inbody720; Biospace, Seoul, Republic of Korea), including hydration status, recent food and drink consumption, physical activity level, and menstrual cycle. However, all participants at the Kangbuk Samsung Hospital Total Healthcare Center underwent bioelectric impedance analysis measurements following the standard protocol, which included an 8-h fasting period and urination within 30 min prior to measurement to enhance the precision of the obtained results. Second, although the observed association has been adjusted extensively for risk factors of decreased BMD, other unmeasured confounders such as vitamin D or vitamin A status may contribute to the association3,35. Third, it is difficult to generalize the findings to the entire adult population of Republic of Korea. Majority of the participants were current employees, or family members of large companies. Furthermore, only a small number of men underwent DXA scanning, resulting in a significantly lower number of male participants included in this study. However, despite the small number of male participants, the results showed an association between reduced risk of increased BMD with high body fat percentage within the normal BMI range. Fourth, while the NBMI-HA group showed a greater prevalence of decreased BMD compared to the obesity group (as seen in Table 2), the risk ratio of decreased BMD for the NBMI-HA group was lower than that of the obesity group when considering only female participants. Given the diverse factors influencing the relationship between fat and bones37, this warrants further investigation.
In conclusion, the incidence of decreased bone density was highest in the NBMI-HA group, and the risk of decreased bone density was statistically significantly higher in the NBMI-HA group than in the NBMI-NA group, regardless of the adjustments made. This suggests that, even if the recorded BMI was normal, a high BFP is associated with an increased risk of decreased bone density. At present, there has been an increase in the number of individuals attempting to manage their health, with most simply focusing on BMI6. However, the results of this study confirm that focusing on a healthy body composition, not simply BMI, is more important in preventing decreased BMD. This could lead to significant implications for the development of effective preventive strategies for osteoporosis.
Data availability
The datasets used and/or analyzed during the current study are not publicly available outside the hospital due to institutional review board limitations, which prevent widespread dissemination of the data. However, the datasets are available from the corresponding author on reasonable request and with permission of the institutional review board.
References
Rodriguez-Gomez, I. et al. Osteoporosis and its association with cardiovascular disease, respiratory disease, and cancer: Findings from the UK Biobank Prospective Cohort Study. Mayo Clin. Proc. 97, 110–121 (2022).
Vilaca, T., Eastell, R. & Schini, M. Osteoporosis in men. Lancet Diabetes Endocrinol. 10, 273–283 (2022).
Kasper, D. et al. Harrison's Principles of Internal Medicine, 19e
Harvey, N., Dennison, E. & Cooper, C. Osteoporosis: A lifecourse approach. J. Bone Miner. Res. 29, 1917–1925 (2014).
Mulugeta, W., Desalegn, H. & Solomon, S. Impact of the COVID-19 pandemic lockdown on weight status and factors associated with weight gain among adults in Massachusetts. Clin. Obes. 11, e12453 (2021).
Boo, S. Body mass index and weight loss in overweight and obese korean women: The mediating role of body weight perception. Asian Nurs. Res. 7, 191–197 (2013).
Premaor, M. O., Comim, F. V. & Compston, J. E. Obesity and fractures. Arq. Bras. Endocrinol. Metabol. 58, 470–477 (2014).
Cheung, Y. M., Joham, A., Marks, S. & Teede, H. The obesity paradox: An endocrine perspective. Intern. Med. J. 47, 727–733 (2017).
Gkastaris, K. et al. Obesity, osteoporosis and bone metabolism. J. Musculoskelet. Neuronal. Interact. 20, 372–381 (2020).
Fassio, A. et al. Correction to: The obesity paradox and osteoporosis. Eat Weight Disord. 23, 303 (2018).
Hannan, M. T., Felson, D. T. & Anderson, J. J. Bone mineral density in elderly men and women: Results from the Framingham osteoporosis study. J. Bone Miner. Res. 7, 547–553 (1992).
Ducy, P. et al. Leptin inhibits bone formation through a hypothalamic relay: A central control of bone mass. Cell 100, 197–207 (2000).
Pfeilschifter, J., Koditz, R., Pfohl, M. & Schatz, H. Changes in proinflammatory cytokine activity after menopause. Endocr. Rev. 23, 90–119 (2002).
Zhao, L. J. et al. Correlation of obesity and osteoporosis: Effect of fat mass on the determination of osteoporosis. J. Bone Miner. Res. 23, 17–29 (2008).
Hsu, Y. H. et al. Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am. J. Clin. Nutr. 83, 146–154 (2006).
Ahn, S. H. et al. Different relationships between body compositions and bone mineral density according to gender and age in Korean populations (KNHANES 2008–2010). J. Clin. Endocrinol. Metab. 99, 3811–3820 (2014).
Oh, S. et al. The association between cotinine-measured smoking intensity and sleep quality. Tob. Induc. Dis. 20, 77 (2022).
Kanis, J. A. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: Synopsis of a WHO report. WHO Study Group. Osteoporos. Int. 4, 368–381 (1994).
Sung, J., Ryu, S., Song, Y. M. & Cheong, H. K. Relationship between non-alcoholic fatty liver disease and decreased bone mineral density: A retrospective cohort study in Korea. J. Prev. Med. Public Health 53, 342–352 (2020).
Namgoung, S. et al. Metabolically healthy and unhealthy obesity and risk of vasomotor symptoms in premenopausal women: Cross-sectional and cohort studies. BJOG 129, 1926–1934 (2022).
Seo, M. H. et al. Prevalence of obesity and incidence of obesity-related comorbidities in Koreans based on national health insurance service health checkup data 2006–2015. J. Obes. Metab. Syndr. 27, 46–52 (2018).
World Health Organization. The Asia-Pacific Perspective: Redefining Obesity and Its Treatment. https://apps.who.int/iris/handle/10665/206936 (2000).
Kanis, J. A. et al. Assessment of fracture risk. Osteoporos. Int. 16, 581–589 (2005).
Kim, Y. M. et al. Variations in fat mass contribution to bone mineral density by gender, age, and body mass index: The Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2011. Osteoporos. Int. 27, 2543–2554 (2016).
Hilton, C. et al. The associations between body fat distribution and bone mineral density in the Oxford Biobank: A cross sectional study. Expert Rev. Endocrinol. Metab. 17, 75–81 (2022).
Addison, O., Marcus, R. L., Lastayo, P. C. & Ryan, A. S. Intermuscular fat: A review of the consequences and causes. Int. J. Endocrinol. 2014, 309570 (2014).
Evans, A. L., Paggiosi, M. A., Eastell, R. & Walsh, J. S. Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J. Bone Miner Res. 30, 920–928 (2015).
Almeida, M. et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol. Rev. 97, 135–187 (2017).
Pasco, J. A. et al. Serum leptin levels are associated with bone mass in nonobese women. J. Clin. Endocrinol. Metab. 86, 1884–1887 (2001).
Ruhl, C. E. & Everhart, J. E. Relationship of serum leptin concentration with bone mineral density in the United States population. J. Bone Miner. Res. 17, 1896–1903 (2002).
Odabasi, E. et al. Plasma leptin concentrations in postmenopausal women with osteoporosis. Eur. J. Endocrinol. 142, 170–173 (2000).
Fasshauer, M. et al. Hormonal regulation of adiponectin gene expression in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 290, 1084–1089 (2002).
Cenci, S. et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J. Clin. Invest. 106, 1229–1237 (2000).
Taguchi, Y. et al. Interleukin-6-type cytokines stimulate mesenchymal progenitor differentiation toward the osteoblastic lineage. Proc. Assoc. Am. Physicians 110, 559–574 (1998).
Chen, C. et al. the Effects of dietary calcium supplements alone or with vitamin D on cholesterol metabolism: A meta-analysis of randomized controlled trials. J. Cardiovasc. Nurs. 32, 496–506 (2017).
Sheu, Y. & Cauley, J. A. The role of bone marrow and visceral fat on bone metabolism. Curr. Osteoporos. Rep. 9, 67–75 (2011).
Ho-Pham, L. T., Nguyen, U. D. & Nguyen, T. V. Association between lean mass, fat mass, and bone mineral density: A meta-analysis. J. Clin. Endocrinol. Metab. 99, 30–38 (2014).
Author information
Authors and Affiliations
Contributions
H.Y. and E.S. conceived and designed the study. H.Y. conducted the experiments and collected the data. H.Y. and M.L. analyzed the data. H.Y., E.S. and S.S. interpreted the results. H.Y. drafted the manuscripts, which was critically revised by E.S. and S.S. All authors approved the final version of the manuscript for submission.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Yoon, H., Sung, E., Kang, JH. et al. Association between body fat and bone mineral density in Korean adults: a cohort study. Sci Rep 13, 17462 (2023). https://doi.org/10.1038/s41598-023-44537-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-023-44537-1
- Springer Nature Limited