lipid profiles and postmenopausal osteoporosis · and osteoporosis susceptibility in postmenopausal...

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Abstract. – OBJECTIVE: To investigate the relationship between blood lipid profiles and os-teoporosis in postmenopausal women.

MATERIALS AND METHODS: A compre-hensive search of the literature related to lip-id profiles and postmenopausal osteoporosis was conducted in Wanfang Database, CNKI, PubMed (1950-2015) and EMBASE (1974-2015). Appropriate studies were selected according to pre-defined exclusion criteria, and the levels of high-density lipoprotein cholesterol (HDL), low-density lipoprotein cholesterol (LDL), tri-glycerides (TG) and total cholesterol (TC) were compared between osteoporosis and normal density groups. Statistical analysis was per-formed using RevMan5.3.

RESULTS: Ten published articles were se-lected for meta-analysis. The results showed that the levels of HDL, LDL, TC were higher in the osteoporosis group than the normal densi-ty group, whereas the levels of TG were lower in the osteoporosis group (HDL: MD = 2.63, 95% CI: 0.43 to 4.84, p = 0.02; LDL: MD = 9.67, 95% CI: -0.10 to 19.44, p = 0.0532; TG: MD = -0.42, 95% CI: -17.52 to 16.67, p = 0.96; TC: MD = 14.82, 95% CI: 2.84 to 26.80, p = 0.02). There was no statistical difference in LDL and TG.

CONCLUSIONS: The serum levels of HDL and TC are higher in postmenopausal osteoporosis patients, and may thus be potentially useful in-dicators to reflect the process of osteoporosis in these women. More research is needed to de-termine the relationship between LDL, TG and postmenopausal osteoporosis.

Key Words:Lipid profiles, Osteoporosis, Postmenopausal wom-

en, Meta-analysis.

Introduction

With the continuous progress of aging, os-teoporosis has become an urgent problem. The results of the 1988-1994 National Health and Nutrition Examination Survey1 showed that os-teoporosis substantially decreased the quality of life in people over the age of 50. With the aging of the population, the incidence of osteoporosis continues to rise, bringing huge economic burden to society and families2,3. The susceptibility of fracture was increased in postmenopausal wom-en with osteoporosis4 and fractures involved high morbidity in population with postmenopausal os-teoporosis (PMOP)5.

A positive association between cardiovascular diseases (CVD) and osteoporosis was supported by epidemiological studies, where cholesterol has been indicated to be a possible link6,7. Tintut et al8 inves-tigated the role of lipids and lipoproteins on bone and a role for atherogenic lipids and lipoproteins in the pathogenesis of bone loss. However, the associ-ation remains unclear. Researchers also show that bone mineral density (BMD) in postmenopausal women is quantitatively associated with blood lipid levels9-13. However, the literature on the relationship between lipids and osteoporosis remains incon-sistent. For example, Li et al14 showed that HDL was positively correlated with postmenopausal os-teoporosis, but LDL, TG and TC were not. Sivas et al15 found a positive correlation between LDL, TC, TG and postmenopausal osteoporosis. Wang et al16 suggested a negative correlation between LDL, TC and postmenopausal osteoporosis, but there was

European Review for Medical and Pharmacological Sciences 2018; 22: 1-9

Y.-Y. CHEN1,2, W.-W. WANG1, L. YANG3, W.-W. CHEN1, H.-X. ZHANG1

1Department of Obstetrics and Gynecology, the First Affiliated Hospital of Nanjing MedicalUniversity, Nanjing, China2Department of Obstetrics and Gynecology, Wuxi Maternity and Child Health Care Hospital, Wuxi,China3Department of Orthopedics, Nanjing First Hospital, Nanjing Medical University, Nanjing, China

Yuanyuan Chen and Weiwei Wang contributed equally to this work

Corresponding Author: Hongxiu Zhang, MD; e-mail: [email protected]; Wenwei Chen, MD; e-mail: [email protected]

Association between lipid profiles and osteoporosis in postmenopausal women: a meta-analysis

Y.-Y. Chen, W.-W. Wang, L. Yang, W.-W. Chen, H.-X. Zhang

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no significant correlation between HDL, TG and postmenopausal osteoporosis. Due to the conflict-ing results and the insufficient statistical power of individual research, a meta-analysis was conducted to elucidate the relationship between serum lipids and osteoporosis susceptibility in postmenopausal women in our study.

Materials and Methods

Search Strategy and Inclusion CriteriaA thorough search of the medical literature was

conducted in Wanfang Database, China National Knowledge Infrastructure (CNKI, 1994-2015), PubMed (1950-2015) and EMBASE (1974-2015), using the key words “lipid profiles,” “osteoporo-sis,” and “postmenopausal women.” The complete retrieval type was as below: (‘osteoporosis’ OR ‘postmenopausal osteoporosis’) AND (‘lipid pro-files’ OR ‘lipids’ OR ‘triglycerides’ OR ‘low-den-sity lipoprotein cholesterol’ OR ‘high-density lipoprotein cholesterol’ OR ‘total cholesterol’). Date of the last search was August 12th, 2015. The studies needed to meet the following criteria: (1) the subjects were human; (2) the studies were ei-ther case-control or cohort studies; (3) the studies focused on the relationship between lipid profiles and osteoporosis in postmenopausal women; (4) subjects in each study were divided into different groups according to their lowest T-score using the WHO classification system: T-score ≥ -1 was regarded as a group with normal BMD, and T-score lower than -2.5 as an osteoporotic group. Included studies only implemented X-ray absorp-tiometry (DEXA) measurements at the lumbar spine. The exclusion criteria were: (1) subjects were not postmenopausal women; (2) publica-tions were duplicated; (3) studies did not contain lipid profile; (4) serious metabolic disease and pa-tients receiving bone active agents, lipid-lowering medication or corticosteroids; (5) the publication was a review article, commentary or case report.

Assessment of Methodology QualityAssessment of the quality of the included stud-

ies was performed according to the following 6 items (Cochrane Handbook for Systematic Re-views of Interventions version 5.1.0).

Data ExtractionObservational Studies in Epidemiology (MOOSE)

guidelines16 was applied in this meta-analysis; the following items were extracted from all including re-

searches: author, publication date, country of origin, number of subjects with osteoporosis and number of normal density subjects, age, duration of menopause, BMI (kg/m2), and BMD evaluation method. First, we reviewed the titles and/or abstract for papers; then, we reviewed the full-text publications. All characteristics were extracted according to a protocol. Publication were excluded if they did not meet the above criteria, and provided insufficient data, for example studies without containing lipid profile.

Statistical AnalysisThe Review Manager Software package (ver-

sion 5.3; the Cochrane collaboration) was used to perform this meta-analysis. For continuous variables, the weighted mean difference (WMD) were measured with the 95% CIs. WMDs were considered statistically significant at the p < 0.05 level. Χ2 and I2 tests were adopted to evaluate the statistical heterogeneity among studies and subgroups. Both fixed-effects (FE) model and a random-effects (RE) model were used to obtain summary WMDs. The FE model was employed with the absence of heterogeneity, otherwise the RE model was employed. Egger’s regression method17 and the Begg-Mazumdar test18 were used to assess the publication bias using the soft-ware Stata 12.0 (Stata Corp LP, College Station, TX, USA). A sensitivity analysis was performed for the HDL, LDL, TC and TG results using Stata 12.0 software.

Results

Study CharacteristicsA total of 526 relevant studies were identified

based on a defined search strategy. By screening the title and abstract, 509 studies were exclud-ed for the following reasons: subjects were not post-menopausal women, the study was review or duplicate, or not cohort or case-control study. Of the remaining 17 articles, two studies were excluded because not all patients met the diag-nostic criteria for osteoporosis. The last five stud-ies were excluded because no usable data were available. Finally, 10 articles13-15,19-25 were eligible for systematic review after critical evaluation. The study selection process is summarized with a flow chart in Figure 1. Our meta-analysis in-volved a total of 3268 participants, including 1016 osteoporosis patients and 2252 healthy women. The main characteristics of the population in the identified studies are summarized in Table I.

Lipid profiles and postmenopausal osteoporosis

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Quality of the Included StudiesA summary of methodological domain as-

sessment for each study is detailed in Figure 2.

Only five studies clearly show the blindness in evaluating the results. In general, the risk of bias is considered low-level.

Meta-AnalysisFirstly, we compared HDL in patients with

osteoporosis to normal controls (Figure 3). There were significant differences in research hetero-geneity when all studies were considered (I2 = 75%, p < 0.0001). The meta-analysis of 10 studies showed a significant increase in HDL levels in the osteoporosis group compared to the normal group (MD = 2.63, 95% CI: 0.43 to 4.84, p = 0.02). Sec-ondly, we compared LDL in osteoporosis cases with normal controls (Figure 4). Similarly, when all studies are considered, research heterogene-ity is also significantly different. (I2 = 95%, p < 0.00001). The meta-analysis of 10 studies showed that the level of LDL in the osteoporosis group was higher than in the normal group. However, in the random effects model, the difference was not statistically significant (MD=9.67, 95% CI:

Figure 1. Flow diagram of the studies identified and reasons for exclusion.

Table I. Characteristics of included studies.

Duration of Number of Age menopause BMI BMD Study Country Groups patients (years) (years) (kg/m2) evaluation

Poli et al20 Italy Osteoporosis 217 55.8 ± 4.5 7.4 ± 5.2 22.9 ± 2.9 BMD was evaluated at Normal 1086 53.8 ±4.1 4.3 ± 3.9 24.4 ± 3.5 the lumbar spine (L2-L4) by DEXACai et al25 China Osteoporosis 69 63.32 ± 6.54 14.8 ± 6.13 24.02 ± 3.74 BMD was evaluated at Normal 51 58.16 ± 5.79 7.29 ± 6.2 25.76 ± 3.69 the lumbar spine (L1-L4) by DEXAChen et al23 China Osteoporosis 30 63.89±6.65 15.59 ± 7.88 24.85±4.79 BMD was evaluated at Normal 30 64.74 ± 6.94 14.81 ± 9.57 23.09 ± 3.64 the lumbar spine (L1-L4) by DEXACui et al24 China Osteoporosis 50 58.02 ± 9.58 13.15 ± 5.64 24.35 ± 4.26 BMD was evaluated at Normal 50 60.82 ± 9.86 8.57 ± 5.04 25.43 ± 4.88 the lumbar spine (L1-L4) by DEXASivas et al15 Turkey Osteoporosis 36 62.8 ± 6.3 17.5 ± 7.4 29.3 ± 4.5 BMD was evaluated at Normal 71 58.6 ± 5.8 11.4 ± 7 32.5 ± 4.4 the lumbar spine (L1-L4) by DEXAD’Amelio et al26 Italy Osteoporosis 101 61.8 ± 6.1 13.1 ± 1.4 23.01 ± 2.2 BMD was evaluated at Normal 72 60.9 ± 6.8 12.9 ± 1.57 23.73 ± 2.04 the lumbar spine (L1-L4) by DEXAPliatsika et al22 Greece Osteoporosis 71 Not provided Not provided Not provided BMD was evaluated at Normal 272 Not provided Not provided Not provided the lumbar spine (L2-L4) by DEXALi et al14 China Osteoporosis 297 64.2 ± 6.3 15.2 ± 7.4 22.5 ± 2.9 BMD was evaluated at Normal 493 61.1 ± 5.8 11.2 ± 6.7 23.9 ± 2.9 the lumbar spine (L1-L4) by DEXAYoldemir et al21 Turkey Osteoporosis 33 51.17 ± 1.4 2.3 ± 0.7 27.2 ± 1.68 BMD was evaluated at Normal 67 51.68 ± 1.05 2.1 ± 0.6 28.32 ± 1.23 the lumbar spine (L1-L4) by DEXAWang et al16 China Osteoporosis 112 66.3 ± 10.2 10.7 ± 4.8 23.5 ± 1.3 BMD was evaluated at Normal 60 65.7 ± 11.5 9.9 ± 4.4 22.7 ± 1.6 the lumbar spine by DEXA


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Figure 2. Quality assessment of the included studies.

Figure 3. Meta-analysis results of HDL levels in osteoporosis cases compared with normal controls. Abbreviations: CI, confidence interval; SD, standard deviation.

Figure 4. Meta-analysis results of LDL levels in osteoporosis cases compared with normal controls. Abbreviations: CI, confidence interval; SD, standard deviation.


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-0.10 to 19.44, p = 0.0532). Thirdly, we compared TG in osteoporosis people with normal controls (Figure 5). Also, a significant difference between study heterogeneity was found (I2 = 94%, p < 0.0001), but the TG level was lower than that of the normal group. However, the difference was not statistically significant under a random effect model (MD = -0.42, 95% CI: -17.52 to 16.67, p = 0.96). Finally, we compared TC in patients with osteoporosis to normal controls (Figure 6). All studies considered significant differences in re-search heterogeneity (I2 = 95%, p < 0.0001). The meta-analysis of 10 studies showed that TC lev-els in postmenopausal women with osteoporosis were statistically significant higher than those in the normal group. (MD = 14.82, 95% CI: 2.84 to 26.80, p = 0.02).

Sensitivity Analysis and Publication BiasThe sensitivity analysis showed that the results

were not disproportionately influenced by any individual study (Figures 7-10). The Egger’s test,

conducted using the same software, revealed the funnel pattern’s symmetry, indicating no evidence of publication bias (p = 0.180 for HDL, p = 0.230 for LDL, p = 0.087 for TC, p = 0.626 for TG).

Discussion

We aimed to investigate whether levels of blood lipid profiles were related to osteopo-rosis in postmenopausal women. This current research suggested that osteoporosis group had significantly higher HDL and TC level than the normal density group. Our present study also showed that the level of TG was lower in the osteoporosis group than in the normal density group, but the difference was not sta-tistically significant. In addition, our results showed that osteoporosis group had a higher LDL level compared with the normal density group. Our findings strongly suggest that high-er HDL and TC were significantly associated

Figure 5. Meta-analysis results of TC levels in osteoporosis cases compared with normal controls. Abbreviations: CI, confidence interval; SD, standard deviation.

Figure 6. Meta-analysis results of TG levels in osteoporosis cases compared with normal controls. Abbreviations: CI, confidence interval; SD, standard deviation.


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with increased osteoporosis susceptibility. We showed that osteoporosis group had a signifi-cant higher HDL level compared to the normal density group. Our reports were consistent with previous findings11,14,20, which observed a posi-tive correlation between serum HDL level and osteoporosis susceptibility. Otherwise, Poli et al20 and Cai et al25 showed no significant asso-ciation between serum HDL level and osteopo-rosis susceptibility.

Elevated levels of LDL in the blood can lead to deposits on the cardio-cerebral vascular ar-eas such as the arterial wall. These gradually form atherosclerotic plaques and can block blood vessels. However, literature on the rela-tionship between LDL levels and osteoporosis remains inconsistent. This controversial link between them could be explained partly by lacing power of individual research. Our me-ta-analysis showed that osteoporosis group had a higher LDL level compared with the normal density group. Sivas et al15, in accordance with

our results, observed that LDL-C were associ-ated with BMD26. Also, Makovey et al27 stated a modest inverse relationship between lumbar spine and the whole body BMD and serum LDL levels in post-menopausal women. Addi-tionally, Wang et al16 and Cui et al24 have shown a negative relationship between them. Other-wise, Li et al14 found that LDL levels were not associated with the risk of osteoporosis.

Total cholesterol (TC) refers to the sum of all lipoprotein cholesterol in the blood. High TC can lead to many diseases such as coronary heart disease, diabetes mellitus, cerebral throm-bosis and stroke. The menopausal bone loss is mainly caused by the lack of estrogen, a steroid hormone that is an esterified form of cholesterol synthesis15. So, the TC levels would be associ-ated with the lower levels of stored estrogen, then affecting the pathogenesis of osteoporosis. Knowing the association between levels of TC and osteoporosis risk in postmenopausal women was very important. Our study found that osteo-

Figure 7. Sensitivity analysis for HDL levels.

Figure 8. Sensitivity analysis for LDL levels.

Figure 9. Sensitivity analysis for TC levels.

Figure 10. Sensitivity analysis for TG levels.


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porosis group had significantly higher TC level compared with the normal density group in post-menopausal women. Also, Sivas et al15 found a positive relationship between them. However, Li et al14 observed no correlation between TC level and osteoporosis susceptibility in postmenopaus-al women. Cui et al23 found a negative relation-ship between LDL level and risk of osteoporo-sis. Additionally, previous studies27 have shown a modest inverse relationship between lumbar spine and serum TC levels in post-menopausal women. Triglyceride (TG) is the most abundant lipid in the human body. Most organs are able to use triglyceride decomposition products to ob-tain energy. Also, the liver and other organs can undertake the synthesis of triglycerides, stored in fat tissue. In order to clarify the relationship between TG levels and osteoporosis risk in post-menopausal women, our present study showed no correlation between TG levels and osteoporosis susceptibility. Our findings were similar with previous studies11,14-16,24. Otherwise, Sivas et al15 found a positive relationship between them. Our research has some unique strengths. This may be the first meta-analysis to illuminate the relation-ship between lipid profiles and postmenopausal osteoporosis. Furthermore, we strictly followed the requirements of meta-analysis and set stan-dard criteria: subjects with effects of lipid or bone altering treatment or serious metabolic disease, were excluded. In addition, all the studies includ-ed the provision of lumbar osteoporosis diagno-sis. Furthermore, BMD was measured by DEXA, thus increasing the credibility of the outcomes. So far, several factors are regarded to affect bone metabolism and increase the risk of bone frac-ture. BMI has been positively linked to BMD, as weight poses a mechanical load on bone, leading to stimulation of bone formation. Obesity also induces hormone-mediated mechanisms, mainly due to insulin resistance and hyperinsulinemia. At the same time, they promote bone turnover by stimulating osteoblast activity and inhibiting bone resorption due to adipocyte-associated hor-mone levels (leptin, estrogen and adiponectin) and other nutrition-related growth factors, rather than by bone-loading effects28. Differences in nu-tritional patterns (insufficient intake of calcium in low-fat diets and hyperlipidemic patients) may also affect bone density. Some studies explain that interweaving bone mass and blood lipids induce lipid oxidation to promote atherosclerosis formation and to divert stromal marrow cells into adipogenesis rather than osteogenesis. As well

as it enhances osteoclastic and impairs osteo-blastic activity, thereby reducing bone formation and increasing bone resorption29. The mevalonate pathway may be the link between lipid profile and bone metabolism, explaining the common effects of statins and bisphosphonate treatment on high lipid profile and osteoclastic apoptosis29,30. The exact causality linking these lipid changes to osteoporosis remains to be determined through further studies in this field. Though we applied a DEXA, a golden standard of BMD measure-ment and a good searching strategy, our study has several limitations. Firstly, lipid profile could observe seasonal variations; however, no subject is stated in the original essay. Secondly, bone mineral density is not only genetically related but also environmental, such as diet and smoking. Our research could not be stratified by factors mentioned above, since primary studies did not provide these data. Lastly, heterogeneity among all the included studies weakened our results to some extent. For these ten publications, five came from China14,16,23-25, two from Turkey15,21, two from Italy20,26, and one from Greece22. Hence, the origin of a population may be a source of heterogeneity. Moreover, age, race and detection methods for different participants also contribut-ed to the heterogeneity. Given this, we performed all meta-analysis using random effects models instead of the fixed-effect model due to high heterogeneity in this work. Therefore, for these reasons, our findings must be taken with caution at the present time.

Conclusions

We provided strong evidence that HDL and TC, but not LDL and TG, were associated with osteoporosis susceptibility in postmenopausal women. The link between them needs to be elu-cidated in future studies. Though defects in lipids metabolism may be genetic, it is involved with nutritional origin. Anyway, our meta-analysis will help clinicians to screen for osteoporosis and lipid changes to osteoporosis, showing a benefit for osteoporosis in postmenopausal women.

AcknowledgementsThis work was supported by the National Natural Science Foundation of China (No. 81472989, to Hong-Xiu Zhang)and the Priority Academic Program Development of Jiang-su Higher Education Institutions.


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Conflict of InterestThe Authors declare that they have no conflict of interests.

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