Meta-analysis of the correlation between BMI and risk factors for osteoporosis

doi:10.21203/rs.3.rs-3249131/v1

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Meta-analysis of the correlation between BMI and risk factors for osteoporosis

https://doi.org/10.21203/rs.3.rs-3249131/v1

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Objectives: The purpose of this meta-analysis is to assess whether there is an association between BMI and osteoporosis.

Methods: Domestic and foreign databases were searched for case-control studies published from 1990.1.1. to 2022.12.31, they use medical subject headings (MeSH) and keywords. All statistical analyses were performed using Review Manager 5.3. If I2 <50%, a fixed-effects model was adopted. If I2> 50% (which indicated great heterogeneity), a random-effects model was adopted.

Results: This meta-analysis included 18 case-control studies covering 9078 individuals, published between 1990 and 2022. The pooling analysis shows that low BMI is a risk factor for osteoporosis complicated by type 2 diabetes, high BMI is a risk factor for osteoporosis complicated by menopausal women, and low BMI is a risk factor for primary osteoporosis. The correlation between normal and high BMI and primary osteoporosis cannot be demonstrated yet; BMI is a risk factor for osteoporosis in patients with frequent glucocorticoid use or COPD, and the correlation between BMI and risk factors for osteoporosis in stroke patients cannot be demonstrated yet.

Conclusions: Our meta-analysis shows that low BMI is a risk factor for osteoporosis complicated by type 2 diabetes and primary osteoporosis, high BMI is a risk factor for osteoporosis complicated by menopausal women, and BMI is a risk factor for osteoporosis in patients with frequent glucocorticoid use or COPD. This provides a theoretical basis for the prevention of osteoporosis in clinical practice.

BMI osteoporosis

risk factors

meta-analysis

Osteoporosis (OP) is a skeletal metabolic disease with reduced bone mass, increased brittleness of bone and easy fracture ^[1]. Osteoporosis is a common and frequent disease in the elderly. It is reported that more than 9 million osteoporotic fractures occur worldwide every year. Once the fracture, especially a hip fracture, the death rate is 23% within one year, so osteoporosis is also called a "silent killer". In some areas of China, the detection rate of OP can reach (294-589) /10,000, OP elderly people are more prone to fracture after a fall, and the annual fracture due to OP in China is about 9.6% ^[2] and a series of problems such as hospitalization, surgery and bed rest for the elderly after fracture, which brings a huge burden to the family and society ^[3]. The incidence of OP is gradually increasing with the changing modern lifestyle and the ageing population; early osteoporosis patients often do not have any clinical symptoms and are easily overlooked. Patients who come to the clinic for pain or brittle fracture have already developed severe osteoporosis once diagnosed ^[4-5], so prevention of osteoporosis has become a top priority.

Osteoporosis includes primary and secondary osteoporosis. Primary osteoporosis includes osteoporosis in elderly men and postmenopausal osteoporosis. Secondary osteoporosis includes osteoporosis caused by various other diseases, including type 2 diabetes, COPD, stroke, spinal cord injury, etc. Clinical studies have shown that increasing age, excessive alcohol consumption, smoking, menopause, and a family history of osteoporosis are risk factors for the development of osteoporosis. In contrast, regular exercise, regular daily sun exposure, and milk consumption are protective factors against the development of osteoporosis^[6]. The correlation between BMI (body mass index) and osteoporosis is currently very controversial. It has been shown that BMI is a protective factor for the development of OP in elderly men in China ^[7]. At the same time, some related studies have demonstrated ^[8] that BMI is not significantly associated with the development of osteoporosis. In order to further prove the correlation between BMI and osteoporosis and provide some reference for people to prevent osteoporosis, this study further clarified the correlation between BMI and osteoporosis in detail through a meta-analysis of related literature at home and abroad.

This meta-analysis was conducted in accordance with the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Page et al., 2021). The protocol was pre-registered in the International Prospective Register of Systematic Reviews (PROSPERO) platform.

Data Sources and Searches

PubMed, Web of Science, Springer Link, China Knowledge Network (CNKI), China Biomedical Literature Database (CBM), Wanfang database and Vipshop series databases were searched for cohort studies published from database inception to 2022.12.31. Language restrictions are English and Chinese. The search strategy combined the use of medical subject headings (MeSH) and keywords. The English search used "BMI" and "osteoporosis" or "bone loss" and "risk factors" or "association factor", "dangerous factors" or "related factors" and "case-control trial" as search terms, and the Chinese search used "BMI" or "body mass index" and "osteoporosis" or "bone loss" and "risk factors" or "influence factors" and "case-control trial" or "clinical trial" as search terms, and the literature search process is shown in Figure 1. other relevant published meta-analyses were also examined to identify relevant trials.

Eligibility Criteria

The trials were included on the basis of the following eligibility criteria:①. the design type was a case-control study; ②. the source of cases was patients with osteoporosis diagnosed in various medical institutions, and the control group was patients who lived in the same area as the cases, based on a larger community population or in the same hospital with similar conditions as the cases described above and admitted at the same time; ③. published literature from January 1, 1990, to December 31, 2022, in domestic and international, involving risk factors including BMI; ④. Data that were available in the study results or could be converted to OR values, 95% CI and standard errors (SE).

Exclusion criteria: ①. duplicate publications; ②. non-Chinese or English literature; ③. literature from the same region in the same year; ④. studies with no control group, incomplete basic data and too many missed visits; ⑤. review literature; ⑥. risk factor definitions differed significantly from the general or most of the study criteria.

Study Selection

Study selection was performed by two reviewers (YanLing Chen and XianBiao Chen) who independently screened the literature based on the eligibility and exclusion criteria. Duplicate and irrelevant articles were first excluded according to their titles and abstracts. After that, the full texts of the potentially eligible articles were downloaded and read to identify all eligible studies. Any disagreements were resolved by the third reviewer (Yunhuo Cai), who acted as an arbiter.

Data Extraction

Data extraction was performed independently by the two reviewers mentioned above (YanLing Chen and XianBiao Chen), who consulted the guidelines on data extraction for systematic reviews and meta-analysis. They used predesigned forms for extracting data, including author, country, time of publication, type of study design, number of cases, number of controls, type of osteoporosis, BMI classification, OR, 95% CI and SE. Disagreements were resolved by discussion with Yunhuo Cai to reach a consensus.

Risk of Bias Assessment

The Newcastle-Ottawa scale (NOS) was used to assess the quality of case-control studies. Stars ranged from 0 to 9 points for case-control studies, four stars for selection of participants and measurement of exposure, two stars for comparability, and three stars for assessment of outcomes and adequacy of follow-up, with more stars indicating higher study quality. Scores of 0–3, 4–6, and 7–9 were considered to indicate low, moderate, and high quality, respectively.

Statistical Analysis

The adjusted OR, 95% CI and SE from each trial were used to assess the association between BMI and Various types of osteoporosis. The χ² -test and the I² -values were used to evaluate heterogeneity. If P> 0.1 and I² ≤ 50%, a fixed-effects model was adopted. If I² > 50% (which indicated great heterogeneity), a random-effects model was adopted. The sensitivity analysis was performed by excluding one study each time and rerunning it to verify the robustness of the overall effects. All statistical analyses were performed using Review Manager 5.3.

Literature Search

The systematic search of case-control studies published from 1990.01.01 to 2022.12.31 identified 998 results. After title and abstract screening, 18 articles were considered potentially relevant. 18 studies (Zou DongMei et al., 2020; Jin Yong et al., 2016; Xiu ShuangLing et al., 2020; Ceng Feng et al., 2022; Zhao Ying et al., 2018; Zhu Bing et al., 2005; Gu QiaoPing et al., 2020; Zhao Yu et al., 2022; Wen HaiZhao et al., 2022; Xiong Jian et al., 2016; Can-Chen Ma et al., 2017; Yu Mor et al., 2020; Chun-Wei Lin et al., 2015; Lidwien Graat-Verboom et al., 2012; Wang Kai et al., 2020; Li HuiLan et al., 2008; Cao Ying et al., 2014; T. S U Z U K I et al., 1997) were included after a full-text review. The selection process is presented in Figure 1.

Study Characteristics

This meta-analysis included 18 case-control studies covering 9078 individuals, which were published between 1990 and 2022, and had clear diagnostic criteria for primary osteoporosis (osteoporosis in older men and postmenopausal osteoporosis) versus secondary osteoporosis. OR,95% CIand SE for the association between BMI and osteoporosis were included in all findings. Two of these papers examined BMI by class (Lidwien Graat-Verboom et al., 2012; Cao Ying et al., 2014). The main characteristics of the included trials are shown in Figure 2.

Quality Assessment

According to NOS criteria, the average score was 7.8 for all included cohort studies, and the score for each trial was seven or above, indicating that all case-control studies were of high quality in this meta-analysis. The scores of the included studies are shown in Figure 2.

BMI and risk factors for osteoporosis in combination with type 2 diabetes

Five case-control studies (Zou DongMei et al., 2020; Jin Yong et al., 2016; Xiu Shuang Ling et al., 2020; Ceng Feng et al., 2022; Zhao Ying et al., 2018) explored the association between BMI and Type 2 diabetes mellitus combined with osteoporosis. The meta-analysis showed that I 2 = 98%. The heterogeneity is large, so the sensitivity analysis uses the method of plural exclusion. They exclude one of the papers (Zhao Ying et al., 2018). The pooling analysis of the remaining four papers shows that BMI is associated with an increased risk of Type 2 diabetes mellitus combined with osteoporosis (OR = 1.92; 95% CI: 1.73–2.21; I 2 = 0%, P < 0.00001; Figure 3). The results showed that low BMI was a risk factor for osteoporosis complicated by type 2 diabetes. After analyzing this literature, the results show that (Zhao Ying et al., 2018; OR=0.85, P=0.045) Low BMI is a risk factor for complications of osteoporosis in patients with type 2 diabetes.

BMI and risk factors for postmenopausal osteoporosis in women

Three case-control studies (Zhu Bing et al., 2005; Gu QiaoPing et al., 2020; Zhao Yu et al., 2022) explored the association between BMI and postmenopausal osteoporosis in women. The meta-analysis showed that I 2 = 87%. The heterogeneity is large, so the sensitivity analysis uses the method of plural exclusion, excluding one of the papers (Zhao Yu et al., 2022). The pooling analysis of the remaining two papers shows that BMI is associated with an increased risk of postmenopausal osteoporosis in women(OR = 0.50; 95% CI: 0.32–0.77; I ² = 0%, P =0.002; Figure 4). The analysis showed that high BMI is a risk factor for osteoporosis in menopausal women; The results of this analysis of the literature (Zhao Yu et al., 2022; OR=2.252, P=0.0431) suggest that a high BMI is a risk factor for complications of osteoporosis in menopausal women.

BMI and risk factors for primary osteoporosis

Four case-control studies (Xiong Jian et al., 2016; Wen HaiZhao et al., 2022; Cao Ying et al., 2014; T. SUZUKI et al., 1997) explored the association between BMI and risk factors for primary osteoporosis. A total of eight studies were involved in the data. The meta-analysis showed I²=65%, which is more heterogeneous, so the sensitivity analysis was done by subgroup analysis according to the grade of BMI (low, normal, high), including data from four studies (Xiong Jian et al., 2016; Wen HaiZhao et al., 2022; Cao Ying et al., 2014; T. SUZUKI et al., 1997). The results of the meta-analysis showed that: OR = 0.59; 95% CI: 0.41–0.85; I ²=43%, P = 0.005; The results of the final analysis study showed that low BMI is associated with an increased risk of primary osteoporosis; Figure 5.

Subgroup 2 consisted of two papers with normal BMI, a total of 2 studies data (Cao Ying et al., 2014; T. SUZUKI et al., 1997); meta-analysis results show: I² = 90%, heterogeneity is considerable. So, it cannot indicate that normal BMI is related to risk factors for primary osteoporosis, Plural analysis of the literature: Results of a literature (Cao Ying et al., 2014) analysis shows that normal BMI is not a risk factor for primary osteoporosis (OR=1.018, =0.9664); An analysis of the literature (T. SUZUKI et al., 1997) shows that normal BMI is a risk factor for primary osteoporosis (OR=0.46, P<0.05).

Subgroup 3 consisted of two papers with high BMI, a total of 2 studies data (Cao Ying et al., 2014; T. SUZUKI et al., 1997). Meta-analysis results show: I ² = 62%, heterogeneity is considerable. So, it cannot indicate that high BMI is related to risk factors for primary osteoporosis, Plural analysis of the literature: Results of a literature (Cao Ying et al., 2014) analysis shows that high BMI is not a risk factor for primary osteoporosis (OR=0.897, =0.7874); An analysis of the literature (T. SUZUKI et al., 1997) shows that high BMI is a risk factor for primary osteoporosis (OR=0.18, P<0.001).

BMI and risk factors for glucocorticoid-induced osteoporosis

Two case-control studies (Can-Chen Ma et al., 2017; Yu Mor et al., 2020) explored the association between BMI and glucocorticoid-induced osteoporosis; The results of the meta-analysis showed that: OR = 0.86; 95% CI: 0.82–0.90; I ²= 0%, P <0.00001; The results of the final analysis study showed that patients with regular glucocorticoid use, BMI is a risk factor for osteoporosis. Figure 6.

BMI and risk factors for COPD combined with osteoporosis

Two case-control studies (Chun-Wei Lin et al., 2015; Lidwien Graat-Verboom et al., 2012) explored the association between BMI and COPD combined with osteoporosis. Three studies data were included in the study; The results of the meta-analysis showed that: OR = 0.30; 95% CI: 0.27–0.34; I ²= 9%, P <0.00001; The results of the final analysis study showed that BMI is a risk factor for comorbid osteoporosis in COPD patients.

BMI and risk factors for stroke combined with osteoporosis

Two case-control studies (Wang Kai et al., 2020; Li HuiLan et al., 2008) explored the association between BMI and stroke combined with osteoporosis. Meta-analysis results show: I²=96%, heterogeneity is large, so it cannot indicate that BMI is related to risk factors for stroke combined with osteoporosis, Plural analysis of the literature: Results of a literature (Wang Kai et al., 2020) analysis shows that low BMI is a risk factor for stroke combined with osteoporosis (OR=2.427, P=0.043); An analysis of the literature (Li HuiLan et al., 2008) shows that low BMI is a risk factor for stroke combined with osteoporosis (OR=0.75, P<0.01).

Publication Bias:

Because the number of papers included in each study did not exceed seven, no test of publication bias was given.

Main Findings:

In this study, a meta-analysis of 18 case-control studies literature with a total of 23 studies was conducted. This study showed that: low BMI is a risk factor for osteoporosis complicated by type 2 diabetes, high BMI is a risk factor for osteoporosis complicated by menopausal women, and low BMI is a risk factor for primary osteoporosis. The correlation between normal and high BMI and primary osteoporosis cannot be demonstrated yet; BMI is a risk factor for osteoporosis in patients with frequent glucocorticoid use or COPD, and the correlation between BMI and risk factors for osteoporosis in stroke patients cannot be demonstrated yet.

Interpretation of Findings: Several meta-analyses at home and abroad have reported the correlation between BMI and risk factors for osteoporosis, and Fu Mengfei et al. ^[9] demonstrated that low body mass index is a risk factor for combined osteoporosis in patients with type 2 diabetes mellitus, which is consistent with the results of the present study; this may be due to the fact that, on the one hand, the mechanical load on the bones of patients with lower body mass index is small, and the relatively small mechanical load can increase bone resorption and leading to the development of osteoporosis ^[10], in addition, obesity has a protective effect on bone density, which may be related to the conversion of testosterone to estradiol and androstenedione to estrone in peripheral adipose tissue of obese patients, which in turn stimulates the secretion of insulin-like growth factor-1 by osteoblasts and promotes bone formation. Yi Zhan et al. ^[11] confirmed that BMI is a protective factor for postmenopausal osteoporosis, but this literature did not specify the grade of BMI because the effects of low and high BMI on postmenopausal osteoporosis in women are different, and this meta-analysis proved that high BMI is a risk factor for concurrent osteoporosis in menopausal women, which may be because body mass index mainly reflects overall fatness and thinness. A proper body mass index can stimulate weight-bearing bone growth and facilitate bone health ^[12], while obesity can lead to a decrease in bone cells and also destroy bone cells through inflammatory factors, leading to osteoporosis ^[13], Xia Xia-Mei et al. confirmed that BMI is a protective factor against osteoporosis in elderly men, while Wang Yu-He et al. confirmed that there is no correlation between BMI and risk factors for primary osteoporosis. The results of domestic and international studies are somewhat divergent regarding the correlation between BMI and risk factors for primary osteoporosis because the effects of different levels of BMI on primary osteoporosis are different. The results of this meta-analysis showed that low BMI was a risk factor for primary osteoporosis, and it could not be proved that normal and high BMI were associated with primary osteoporosis. It can be due to the fact that BMI is most often used to determine the nutritional status of the human body and is positively correlated with BMD, lower body weight reduces the load on the bones of the body, and the amount of bone mineral in the human body decreases with the amount of fat, and under the constant stimulation of low body weight, BMD remains at a lower level and leads to the occurrence of osteoporosis; Zhang Ning et al. ^[14] confirmed that BMI is a risk factor for COPD combined with osteoporosis, which is consistent with the results of this meta-analysis, and some studies have shown that low body mass index in COPD patients is caused by abnormal bone metabolism caused by elevated levels of TNF-α and cytokines and oxidative stress ^[15], but the extent to which it promotes the correlation between COPD patients and BMI needs further study ^[16], the correlation between BMI and risk factors for concurrent osteoporosis in stroke patients has not been reported in the home and abroad literature and the results of this meta-analysis study do not yet prove that BMI is a risk factor for concurrent osteoporosis in stroke patients.

Implications and Limitations:

The results of the present study have their own limitations, which are mainly manifested in some literature results that do not distinguish between BMI grades, which affects the rigour of the results of the present meta-analysis, because the effect of low or high BMI on osteoporosis risk factors is different; on the other hand, for the literature studies with BMI grades, the criteria for BMI grades (low, normal, high) differ slightly in each literature, This also affects the rigour of the results of this meta-analysis to some extent. Thirdly, the literature

of this study was small, and the correlation between normal and high BMI and primary osteoporosis risk factors and the correlation between BMI and stroke combined with osteoporosis could not be analyzed because of the large heterogeneity of the results. In future research, we will search for more literature to find the criteria that meet the BMI classification and explore the correlation between different grades of BMI and risk factors of osteoporosis to provide theoretical support for future clinical prevention of osteoporosis.

This meta-analysis suggests that low BMI is a risk factor for osteoporosis complicated by type 2 diabetes, high BMI is a risk factor for osteoporosis complicated by menopausal women, low BMI is a risk factor for primary osteoporosis, BMI is a risk factor for osteoporosis in patients with frequent glucocorticoid use or COPD. However, more studies are still needed to confirm the correlation between normal and high BMI and primary osteoporosis and the correlation between BMI and risk factors for osteoporosis in stroke patients; The results of our meta-analysis can be very useful in preventing osteoporosis.

Ethics approval and consent to participate：

Because this article does not involve human trials, there are no ethical issues.

Consent for publication:

Not applicable

Acknowledgments:

The authors express their gratitude to YiChen Gong and Yun Huo Cai for their continuous and priceless help during this study.

Availability of data and materials :

The datasets used during the current study are available from the corresponding author on reasonable request(By E-mail:[email protected]).

Authors' contributions:

Ning Li was responsible for the writing and statistical analysis of the articles, Yichen Gong was responsible for the selection and collection of the literature, and Yunhuo Cai gave us assistance and support in statistical analysis.

Funding:

This research received no specific grant from any funding agency in the public,commercial ,or not-for-profit sectors.

Competing interests:

The authors declares that there is no conflict of interest.Ning Li has not received any consulting fees or lecture fees,YiChenGong and Yun Huo Cai has nothing to disclose. Ning Li has full access to all the data in the study and has final responsibility for the decision to submit for publication.

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No competing interests reported.

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Meta-analysis of the correlation between BMI and risk factors for osteoporosis

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