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63 (); 70-76
doi:
10.1016/j.jor.2024.10.041

The low bone mass density in adults with hypertension: A meta-analysis

, , , ,
a Department of Radiology, Obstetrics & Gynecology Hospital of Fudan University, Yangtze River Delta Integration Demonstration Zone (QingPu), Shanghai, 201713, PR China
b Department of Radiology, Obstetrics and Gynecology Hospital, Fudan University, Shanghai, 200011, PR China
c Department of Radiology, Shanghai First Maternity and Infant Hospital, Shanghai Tongji University School of Medicine, 201204, PR China

⁎Corresponding author: Xiaomei Tian. qingpuradiology@163.com

⁎⁎Corresponding author: Guofu Zhang. guofuzh@fudan.edu.cn

Received: , Accepted: ,
Professor P K Surendran Memorial Education Foundation
Disclaimer:
This article was originally published by Reed Elsevier India Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Abstract

Osteoporosis and hypertension are frequently co-occurring disorders which cause significant challenges to the public health. According to some researches, adult persons with hypertension often have low bone mass density (BMD). However, there are discrepancies in the reported results. Thus, the primary objective of our meta-analysis is to explore the potential link between low BMD and hypertension in adults.

Two authors systematically carried out a comprehensive review of the available literature on the connection of BMD and hypertension by retrieving PubMed, Web of Science, Cochrane and Embase up to March 2024. The confidence intervals (CIs) and odds ratios (ORs) and were estimated utilising the random effect model. Heterogeneity, subgroup analysis, sensibility analyses and publication bias were performed.

13 studies from the 6080 unique records were analyzed. Pooled analysis revealed that the danger of low BMD was significantly elevated in hypertensive patients than in non-hypertension (OR 1.33, 95 % CI 1.17–1.53, I2 = 79.9 %, p < 0.01). Subgroup analysis revealed a more pronounced link between low BMD and hypertension in the untreated hypertension group (OR 1.64, 95 % CI 0.45–6.02) as opposed to the cohort receiving antihypertensive medication (OR 1.32, 95 % CI 1.16–1.51). The studies carried out in Europe were consistent with those of studies conducted in Asia and North America.

Low BMD is associated with hypertension in adults. Nevertheless, it remains uncertain whether this finding is influenced by shared risk factors, given the considerable heterogeneity between study types and methodologies. Further extensive epidemiological documents are necessary.

Keywords

Low bone mass density
Osteoporosis
Hypertension
Meta-analysis
1

1 Introduction

Osteoporosis refers to a bone disorder identified by a reduction in bone mass, microstructure, and osseous tissue.1 Due to changing modern lifestyles and a growing elderly population, hypertension and osteoporosis have considerably increased morbidity and mortality.2,3 In China and around the world, they typically develop as comorbidities and cause remarkable public health problems.4 According to a study in 2016, the incidence of osteoporosis has grown from 14.94 % to 27.96 % in the preceding decades.5 More importantly, the global prevalance of hypertension may increase from 26.4 % to 29.2 % by 2025.6 Osteoporosis causes deformity, disability, severe pain, and early mortality in elderly individuals.3 High blood pressure and its complications contribute significantly to death and disability, accounting for 9.6 million deaths annually,7 including stroke, heart attack, blindness, renal insufficiency, cognitive adisability and so on.8,9 Hypertension correlates with calcium metabolism disorder and increased urine calcium loss, resulting in an imbalance of calcium in skeletal reconstitution and an increased of enhanced parathyroid hormone, which decrease bone mass and speed up bone turnover.10,11 Furthermore, epidemiological studies12 have shown that a number of variables, including smoking, age, inadequate calcium intake, physical inactivity, and deficiencies in vitamin K and D increase the risk of low bone mass in hypertensive population. A substantial number of observational studies reported that hypertensive sufferers experienced bone mass density (BMD).13,14 However, a national survey carried out by Mussolino et al.15 revealed that no discernible association was detected between high blood pressure and low BMD. The previous meta-analyze conducted by Ye's16 did not provide a clear definition of low BMD. Furthermore, they only included literature on Dual Energy X-ray Absorption (DEXA) methodology for BMD, which had inherent limitations. To establish an unambiguous correlation between them, we performed a comprehensive meta-analysis involving all published data to examine whether low BMD is substaintially linked with hypertension.

2

2 Methods

The current analysis was devised, conducted and reported in adherence to the guidelines of the Systematic Review and Meta-Analysis (PRISMA).17 Our study protocol has been formally registered in the PROSPERO with the ID of CRD42024529888.

2.1

2.1 Search strategy and data source

We retrieving PubMed, Web of Science, Cochrane, Embase from inception data to March 1, 2024. No funding was provided for this analysis. Search key phrases and headings for medical topics included (“osteopenia” or “osteoporosis” or “low BMD” or “low bone mineral density” or “bone loss”) AND (“high blood pressure” or “hypertension” or “high blood pressures”). Only English language papers were selected, and EndNote software X9 (Clarivate Analytics, Philadelphia, PA, USA) was used to handle the materials.

2.2

2.2 Study selection

Low BMD was defined with BMD T value under −1 15. Hypertension was known as systolic arterial pressure ≥140 mmHg and/or diastolic blood pressure ≥90 mmHg or a history of anti-hypertensive drugs.18 The meta-analysis of included studies must fulfill the following inclusion criteria: (1) the primary objective was to report any relevancy between low BMD and hypertension; (2) observational studies (cross-sectional study, case-control study, cohort); and (3) the odds ratio (OR), hazard ratio (HR), or relative risk (RR) with 95 % confidence intervals (CIs) was recorded or the investigation afforded adequate details for these figures to be calculated. The exclusion criteria were: (1) not English or other language publications; (2) review, letter, conference abstract, case report and non-human studies; (3) involving diseases affecting bone metabolism, such as renal disorders, hormone replacement treatment or the administration of any steroids or drugs with the potential to affect skeletal metabolism; and (4) study population under the age of 18 [Fig. 1]. shows the selection process of the included papers.

Search strategy flowchart.
Fig. 1 Search strategy flowchart.
2.3

2.3 Data extraction process and items

Two reviewers GY (with seven years of professional experience) and TXM (professor and head of the department) independently and methodically evaluated the systematically searched titles and abstracts using a standardized form. The selection of literature was conducted in a stepwise manner, initially guided by the abstract and title, then immediately followed full-text browsing. The catalogue of reference literature were also manual retrieved and assessed to identify additional reference materials. Two independent reviewers subsequently carried out the data extraction into a pre-designed data collection form. The following data were retrieved from each pertinent study: first author's name, country, published year, study type, amount of cases, gender, age, low BMD and hypertension prevalence, BMD measurement methods and locations. Multivariable analysis of controlled factors, OR, HR or RR and their 95 % CI. Differences of opinion were settled through consensus.

2.4

2.4 Quality assessment of included studies

One reviewer (GY) evaluated the methodological quality of the 13 literature in our review. The Newcastle-Ottawa Scale (NOS) was appropriated for evaluate the quality of the literature in case-control studies.19 NOS cosist of four points for choosing, two for comparison, and three for exposure or outcomes. Low-, mild-, and excellent-quality studies were rated 0–3, 4–6, and 7–9.20 The reliability of the cross-sectional study were checked out via an 11-items assessment formulated by the Agency for Healthcare Research and Quality (AHRQ).21 An item would receive “0” if the response was “NO” or “UNCLEAR”, and “1” if the reply was “YES”. Essay quality was evaluated using the following scale: low (range 0–3); moderate (range 4–7); high (range 8–11).21

2.5

2.5 Data synthesis and analysis

All data analysis was calculated with Stata® 16.0 and Revman5.3. The heterogeneity across the various researches was assessed by Cochran's Q test and I2 statistics.22 The statistical heterogeneity threshold of Cochran's Q test was P < 0.1. The I2 statistics value of 25 %, 50 % and 75 % was classified the adjectives low, mild, and high heterogeneity.22

Considering the anticipated heterogeneity, a randomized effect model was chosen to evaluated the pooling of studies and effect size.23 Subgroup analyses were evaluated to show the magnitudes of the effects in different subgroups.

Sensitivity analyze was performed to determine the overall ORs influencing factors. Egger's and Begg's test showed that p > 0.05 represented no considerable publication bias.24 The symmetry of funnel plots and no figure absence indicate that there is no evidence of publication bias. P value of less than 0.05 was deemed to be statistically significant.

3

3 Results

3.1

3.1 Study characteristics

Our systematic search identified 14270 unique records (PubMed = 3888, Web of science = 4083, Cochrane = 399, Embase = 5900), after removing 8190 duplicate studies, 6080 studies were retained. Further 5993 records were discounted during the titles (5626) and abstracts (367) screening procress. A comprehensive review of the remaining 87 studies were conducted, of which 74 were furthered excluded: (1) 9 reviews; (2) 3 case reports and 62 articles failed to report any association between low BMD and hypertension. In total, 13 relevant papers25–37 were incorporated into the meta-analysis, including 2 case-control study and 11 cross-sectional study. Table 1 outlined the key characteristics of the included researches. These 13 studies were conducted in Europe (2), Asia (6), North American (4) and Africa (1). The sample size ranged from 122 to 18347. There were 38671 individuals and 71 % were female. In the study cohort, the prevalence of low BMD ranged from 18 % to 75 %, while the hypertension prevalence ranged from 16 % to 67 %. Two methods were used to evaluate BMD among the participants, Standardized Quantitative Ultrasound (QUS) (n = 3), DEXA scanning (n = 8), and the lumbar spine was the most common site (n = 8). The quality scores of 13 articles exhibited a rang from 6 to 9, 4 were moderate and 9 were high quality studies.

Table 1 Characteristics of studies of low BMD and hypertension included in the meta-analysis.
Author（year） Country Study Design Age (years) Subject (Male/Female) HTN Low BMD BMD Method BMD Location Adjustment variables Quality score OR 95 % CI
Pérez-Castrillón, J(2003)25 Case-ControlSpain 36–76 122 (0/122) 67 % 23 % DEXA Lumbar Spine N/A 6a 0.84 (0.35–2.05)
Sumino,H(2008)26 Cross-sectionalJapan 43–77 175 (0/175) 61 % 75 % DEXA Lumbar Spine Age, BMI, years since menopause, estradiol, triglyceride, low-density lipoprotein cholesterol, fasting plasma glucose, the use of antihypertensive drugs and statins 8b 1.34 0.67–2.67)
Kaplan, S(2010)27 Cross-sectionalUSA ≥40 4058 (0/4058) 29 % 64 % DEXA proximal femur Age, Race, BMI, hormone therapy, smoking status, physical activity, dietary calcium and sodium Intake, age at last menstrual period, the use of antihypertensive drugs 9b 1.77 (1.53–2.05)
Javed,F(2012)28 Cross-sectionalUSA ≥60 965 (0/965) 65 % 68 % DEXA Femoral neckLumbar Spine History of diabetes, smocking, corticosteroid use and history of thiazide diuretic use 7b 0.97 (0.73–1.28)
Varenna,M(2013)29 Cross-sectionalItaly ≥50 3301 (0/3301) 25 % 26 % DEXA Lumbar Spine Age, BMI, age at menopause, age at menarche, physical inactivity, high caffeine intake, smoking 7b 1.64 (1.38–1.94)
Mahboub,SM(2015)30 Cross-sectionalEgypt ≥18 153 (0/153) 16 % 30 % QUS Foot Age, number of co-morbidity, parity, fertility period, gynaecological age, enopausal duration 7b 3.18 (1.32–7.69)
El-Bikai, R(2015)31 Cross-sectionalCanada 40–70 n = 18347(51.5) 32 % 18 % QUS Foot Age, sex, BMI, body height, antiosteoporotic medications, antihypertensive medications, cardiovascular diseases 9b 1.28 (1.18–1.38)
Zhang J(2015)32 Cross-sectionalChina 30–90 1878 (0/1878) 45 % 28 % QUS Foot N/A 9b 1.36 (1.11–1.67)
Park,JS(2015)33 Cross-sectionalKorea ≥50 1664 (0/1664) 18 % 38 % DEXA Femur and Lumbar Spine Age, waist circumference, BMI, parathyroid hormone, alkaline phosphatase, total cholesterol and calcium intake 9b 1.35 (1.05–1.73)
Hijazi，N(2020)34 Cross-sectionalSyria ≥40 813 (0/813) 48 % 69 % DEXA Lumbar Spine and Left hip N/A 8b 0.81 (0.60–1.09)
Hao Chai(2021)35 Case-ControlChina 41–90 2039 (0/2039) 18 % 33 % DEXA Femoral neck and Lumbar Spine Age, height, weight, BMI, menarche age, menopausal age, drinking tea, drinking milk, hypertension, and coronary heart disease 8a 1.59 (1.26–2.01)
Wu,Hai-Long(2022)36 Cross-sectionalChina 50–80 n = 850(73.6) 50 % 66 % DEXA Lumbar Spine and Left hip N/A 8b 1.66 (1.25–2.22)
Shuna-Li(2023)37 Cross-sectionalUSA males ≥50 and postmenopausal females 4306 (2208/2098) 57 % 43 % DEXA Femur neck Age, race/ethnicity, marriage, BMI, family PIR, education, recent smoking status, physical activity, total calcium, arthritis, congestive heart failure, coronaryheart disease, angina/angina pectoris, heart attack, and stroke 9b 1.05 (0.93–1.19)
3.2

3.2 Risk of hypertension and low BMD

The correlation between hypertension and low BMD were revealed in [Fig. 2]. The low BMD prevalence in hypertensive individuals was significantly higher than that observed in non-hypertensive population (OR 1.33, 95 % CI 1.17–1.53). The I2 was 79.9 % (p < 0.01).

Forest plot of low BMD and hypertension of 13 independent studies.
Fig. 2 Forest plot of low BMD and hypertension of 13 independent studies.
3.3

3.3 Subgroup analyses

In order to detect potential sources of statistical heterogeneity and assess the reliability of results in this manuscript, we additionally conducted subgroup analysis on the parts of BMD measuring methods, geographic region, study type, use of antihypertensive drugs, sample size and whether to control confounding factors. Table 2 demonstrated the findings of subgroup analysis. The subgroup analysis examined studies using DEXA and QUS independently. Both imaging modalities tended to show a correlative relationship between low BMD and hypertension (DEXA: OR 1.30, 95 % CI 1.08–1.57, p < 0.01 and QUS: OR 1.36, 95 % CI 1.13–1.64, p < 0.01). There were no notable discrepancies between QUS and DEXA (p = 0.75) (Supplementary Material 1). A second subgroup analysis based on geographic regional variation was consistent in Asia, Europe, North America and Africa, and a favourable correlation between low BMD and hypertension was observed. No significant differences were found among those four continents (p = 0.25) (Supplementary Material 2). A third subgroup analysis based on study type revealed no significant distinction between the case-control and cross-sectional research (p = 0.89), (Supplementary Material 3). A subsequent subgroup analysis based on use of antihypertensive drugs revealed a positive relationship between low BMD and hypertension (Supplementary Material 4). The connection between low BMD and hypertension was more pronounced in no antihypertensive drugs (OR 1.64, 95 % CI 0.45–6.02) than in antihypertensive drugs (OR 1.32, 95 % CI 1.16–1.51). After controlling the confounding factors, the OR was 1.38 (95 % CI 1.19–1.62) in low BMD sufferers with hypertension, which was slightly higher than that non-control of confounding factors (OR 1.18, 95 % CI 0.84–1.67) (Supplementary Material 5). Additional subgroup analysis based on sample size (Supplementary Material 6) did not show any statistically significant results neither.

Table 2 Subgroup analyses on the association of low BMD and hypertension.
Subgroup Studies,N OR 95 % CI Heterogeneity across the studies
BMD measurement method I2(%) P value
DEXA 10 1.30 1.08–1.57 84.0 <0.01
QUS 3 1.36 1.13–1.64 54.0 0.11
Study area
Europe 2 1.36 0.76–2.44 52.0 0.15
Asia 6 1.33 1.09–1.62 67.0 = 0.01
North American 4 1.25 1.00–1.56 91.0 0.07
Africa 1 3.18 1.32–7.69 N/A N/A
Study type
Cross-sectional 11 1.40 1.23–1.60 79.0 <0.01
Case-control 2 1.35 0.78–2.32 45.0 0.18
Confounding factors control
Yes 9 1.38 1.19–1.62 83.0 <0.01
No 4 1.18 0.84–1.67 77.0 <0.01
Sample size
Small sample size (n ≤ 200) 3 1.52 0.75–3.08 56.0 = 0.1
Large sample size (n > 200) 10 1.36 1.19–1.56 77.0 <0.01
Use of anti-hypertensive drugs
Yes 11 1.32 1.16–1.51 82.0 <0.01
No 2 1.64 0.45–6.02 77.0 = 0.04
3.4

3.4 Sensitivity analysis and publication bias

Further sensitivity analysis (Supplementary Material 7) showed that those five studies (Kaplan S et al., Javed F et al., Varenna M et al., Hijazi N et al. and Shuna-Li et al.) contributed the most to the heterogeneity. Then, a post-hoc meta-analysis revealed a satisfied size (OR 1.40, 95 % CI 1.25–1.56, p < 0.01) with no significant heterogeneity I2 = 33.3 %, P=0.16) [Fig. 3].

Post-hoc meta-analysis after removing 5 heterogeneous literature.
Fig. 3 Post-hoc meta-analysis after removing 5 heterogeneous literature.

In our present systematic review and meta-analysis, we discovered no evidence of potential publication bias for low BMD and hypertension. The funnel plot [Fig. 4] was symmetrical. Begg's (p = 0.76) and Egger's test (p = 0.74) as well verified the eleven studies were free of publication bias.

Funnel plot of low BMD and hypertension of 13 independent studies.
Fig. 4 Funnel plot of low BMD and hypertension of 13 independent studies.
4

4 Discussion

The findings of our meta-analysis of 13 published studies indicate that a significantly positive connection between low BMD and hypertension. According to sensitivity analysis, our findings appeared to be robust. The funnel plot demonstrated that there was no published bias, reflecting our findings were reliable. However, our meta-analysis revealed considerable statistical heterogeneity and could not be explained by subgroup analyses. The inclusion of five studies (Kaplan S et al., Javed F et al., Varenna M et al., Hijazi N et al. and Shuna-Li et al.) appeared to be the source of heterogeneity. Unfortunately, it is indistinct why these five investigations produced such significant heterogeneity. All these five studies were cross-sectional and used DEXA to evaluate BMD, and there were no significant changes in technique among them. Nevertheless, subgroup analysis based on the testing methods for BMD and study type revealed that these two factors were not the source of heterogeneity. Due to the varied sample size and the inaccessible source of individual data for each trial, there may be clinical heterogeneity and analysis was difficult to be done further. After eliminating these five trials,27–29,34,37 the direction and magnitude of the effect size remained consistent, and heterogeneity disappeared.

The underlying pathophysiological mechanisms connecting low BMD and hypertension in humans remain poorly understood. Numerous studies of clinical, animal, and evidence of epidemiological have demonstrated that hypertension is associated with abnormalities in calcium metabolism, including an increase in urinary calcium excretion38 and parathyroid hormone (PTH) levels,39 as well as a notable trend of low serum free calcium ion levels.40,41 According to a Japanese study, women individuals with high blood pressure had significantly higher urine calcium excretion and lower serum ionized calcium than normotensive people.41 The more urinary calcium excreted, the poorer bone mineral density was found.42

Long-term calcium leakage may contribute to an increased migration of calcium from bone, increasing the risk of osteoporosis. Furthermore, an increase in PTH levels may hasten bone turnover and diminish bone mass, particularly in women.43 Besides, previous studies have found that in hypertensive individuals, the renin-angiotensin system (RAS) was over expressed.44 The level of angiotensin II increased and differentially regulated the differentiation of osteoblasts and osteoclasts, resulting in enhanced bone resorption and decreased bone formation, thus accelerating the process of osteoporosis.44 In females, estrogen deficiency may partially explain why low BMD is correlated with hypertension.45 According to a survery on the connection between estrogen and women's blood pressure, the lower the postmenopausal women's serum estrogen levels, the higher the blood pressure.46 A previous study showed that a number of pathological conditions were related to osteoporosis and hypertension, including abnormal lipid metabolism, modified High Density Lipoprotein (HDL) and Low Density Lipoprotein (LDL), plasma homocysteine, and Nitric Oxide (NO) levels.47 Additionally, a vitamin D shortage can activate the RAS, and the latter can increase parathyroid hormone emission and decrease calcium absorption, then leading to high blood pressure and osteoporosis.48

Subgroup analysis could not explain the heterogeneity. In the subgroup analyses stratified by bone density test, significant statistical heterogeneity was found in DEXA compared to QUS. This may be due to the fact that DEXA was a two-dimensional measurement and is sensitive to degenerative disease which could lead to an overestimation of areal density.49 In subgroup analyses classified on region, statistical heterogeneity was lower in European compared to the other three areas, which may be explained by European genetic factors as well as dietary habits and lifestyle.50 A moderate statistical heterogeneity was exhibited in cross-sectional studies while no statistical heterogeneity was identified in case-control studies. This difference may be attributed to the multiple factors of disease can be easily studied simultaneously in case-control studies other than cross-sectional studies.

4.1

4.1 Limitations

Several limitations of our current meta-analysis should be acknowledged. First, the main limitation of our meta-analysis is the heterogeneity observed across all included studies. Statistical heterogeneity was high at 79.9 % (Fig. 2). Subgroup analysis were remained unaccounted for this heterogeneity. In light of the observational nature of included studies and the differing confounders across the five literature as well as the subsequent considerable statistical heterogeneity, we cannot currently determine the underlying cause of association between low BMD and hypertension. Second, in light of the existing research literature, our meta-analysis comprises only cross-sectional and case-control studies, further cohort studies may be required to raise the level of evidence. Third, because fewer men were included in the studies and could not be extrapolated from the research data, we failed to conduct subgroup analysis according to the gender, which could be a source of heterogeneity. Thus, further investigations including men are required to confirm our findings. Fourth, the sample size in our analysis varied greatly from 122 to 18347, which may lead to the observed heterogeneity. Furthermore, our study was limited to English language papers, which indicated that potential studies conducted in other languages might have been omitted.

4.2

4.2 Conclusion

This meta-analysis demonstrated that the hypertensive individuals have a higher risk of low BMD than that of normotensive individuals. Further studies on the underlying reasons of low BMD are needed for better prevention and intervention of low BMD in hypertensive patients.

Guardian/Patient's consent

This is a meta-analysis exempted from informed patient consent and ethical review.

CRediT authorship contribution statement

Yao Gao: Conceptualization, Methodology, Writing – original draft, Writing – review & editing, Visualization, Supervision, Project administration. Xiaomei Tian: Writing – original draft, Writing – review & editing, Supervision, Project administration. Guofu Zhang: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing – original draft, Writing – review & editing, Visualization, Supervision, Project administration, Writing – original draft, Writing – review & editing, Supervision. Jianli Yu: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing – original draft, Writing – review & editing, Visualization, Supervision, Project administration. Liwen Zhang: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing – original draft, Writing – review & editing, Visualization, Supervision, Project administration.

Ethical statement

This is a meta-analysis exempted from informed patient consent and ethical review.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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