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Prevalence and risk factors of osteoporosis in lupus nephritis patients in China: a cross-sectional study

BMC Nephrology volume 25, Article number: 428 (2024) Cite this article

Abstract

Background

Osteoporosis is a significant concern among individuals with lupus nephritis (LN), with reported prevalence rates exhibiting considerable variation. This study investigates the prevalence and identifies risk factors contributing to osteoporosis in premenopausal and postmenopausal LN patients, addressing the paucity of data specific to the Chinese population.

Methods

This cross-sectional study enrolled patients with renal biopsy-proven LN, who underwent bone mineral density (BMD) measurements using dual X-ray absorptiometry at the lumbar spine, total hip, and femoral neck. The study was conducted at Tongji hospital from May 2011 to June 2018.

Results

A total of 130 patients were evaluated, with a mean age of 46.2 ± 12.9 years, including 2 males and 128 females. A significant majority, 52.3% (n = 67) of the female patients, were identified as postmenopausal. BMD measurements revealed that 40.0% of patients had osteoporosis in at least one site. The spearman rank correlation of BMD with clinical characteristics indicated that age at menopause, weight, height, and body mass index were positively correlated with BMD, while age, age at diagnosis of LN, and menopause duration were negatively correlated with BMD in lumbar spine, total hip, and/or femoral neck. Multivariable linear regression analysis demonstrated that body mass index was positively associated with BMD, whereas disease duration and menopause duration were negatively associated with BMD in all and postmenopausal patients. Postmenopausal patients consistently had a higher prevalence of osteoporosis across all measured sites. Factors such as older age, lower weight, and the absence of bisphosphonates therapy were independently associated with an increased risk of osteoporosis in LN patients.

Conclusion

Our findings underscore a substantial prevalence of osteoporosis in LN patients, especially among postmenopausal individuals. The study identifies older age, lower weight, and absence of bisphosphonates treatment as risk factors for osteoporosis in this patient population.

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Introduction

Systemic lupus erythematosus (SLE) is an autoimmune disorder characterized by multisystemic damage, leading to significant health issues [1]. There is growing concern over the adverse effects of medications used to treat SLE and the potential long-term complications [2]. Lupus nephritis (LN) is a severe and frequently manifestation of SLE, associated with significant morbidity and mortality [3,4,5]. Research indicates that female patients with SLE are at a higher risk of developing reduced bone mineral density (BMD) [6,7,8,9]. Moreover, women exhibit a high prevalence of osteoporosis and osteoporotic fractures [10]. Osteoporosis is a common and serious complication of SLE, contributing to increased morbidity and mortality rates [11, 12]. The reported frequency of osteopenia in SLE patients, according to WHO criteria, ranges from 24 to 74% [13, 14], while osteoporosis affects between 1.4% and 68.7% of patients [9, 15, 16]. Despite these statistics, there is a notable gap in the literature regarding osteoporosis prevalence among Chinese LN patients. Risk factors such as glucocorticoid therapy, early menopause, and low calcium and vitamin D intake are known to contribute to bone loss [17,18,19,20], yet the specific risk factors associated with osteoporosis in LN patients vary by country, indicating a need for further research in this area.

Accordingly, this research endeavor sought to ascertain the prevalence of osteoporosis and identify the risk factors associated with it within a group of Chinese LN patients, presenting these data separately for pre- and postmenopausal individuals to address the paucity of data specific to the Chinese population.

Materials and methods

Patients and experimental design

This single-center, cross-sectional study enrolled LN patients diagnosed through biopsy at Tongji Hospital affiliated with Tongji Medical College, Huazhong University of Science and Technology. The study period spanned from May 1, 2011, to June 30, 2018. All participants provided informed consent to participate. The study protocol was approved by the Ethical Committee of Tongji Hospital Affiliated to Tongji Medical College, Huazhong University of Science and Technology (Project No. TJ-IRB20181106). The exclusion criteria were as follows: pregnancy, and untreated hypothyroidism.

Clinical information was collected, including ethnicity, age at enrollment, menstrual status, age at menopause, personal history of fractures, alcohol consumption, smoking status, and laboratory investigations, such as serum creatinine, uric acid, urea nitrogen, and serum ionized calcium. Anthropometric measurements including weight, height, and body mass index (BMI) were also taken. Information on disease duration, calcium supplements, anti-osteoporotic therapy, and corticosteroid use history were recorded, noting the maximum and current dosages. Disease activity was scored using the Systemic Lupus Erythematosus Disease Activity Index (SLEDAI) [21], and disease damage was assessed based on the criteria established by the Systemic Lupus International Collaborative Clinics/American College of Rheumatology (SLICC/ACR) [22] by the physicians responsible for the patients.

BMD measurements

Skilled technicians performed bone mineral density (BMD) assessments on the lumbar spine (L1-L4), total hip, and femoral neck using a consistent dual-energy X-ray absorptiometry (DXA) device, the Delphi W (serial number 71271), for all patient examinations. The BMD measurements were expressed in grams per square centimeter and T score, which were subsequently juxtaposed with an age-matched female reference population through Z scores. The bone densitometer’s precision, measured by the coefficient of variation (CV%), was as follows: 1.14% for the lumbar spine, 1.91% for the femoral neck, 1.03% for the total hip, and 0.77% for the whole body. BMD values that fell below − 2.5 standard deviations, denoted as T score ≤ -2.5, were classified as indicative of osteoporosis.

Statistical analysis

Kolmogorov-Smirnov test was employed to verify the normality of variable distributions. Categorical variables were expressed as percentages, while normally distributed continuous variables were reported as mean ± standard deviation (SD), and non-normally distributed continuous variables were depicted using the median and interquartile range (IQR). To compare values between two groups, we selected appropriate statistical tests, including two-tailed Student’s t-test, Mann-Whitney U test, Fisher’s exact test, Chi-square with Yates’ correction, or Chi-square test, based on the distribution of the data and the type of variables. Univariate logistic regression analysis was conducted to identify factors that might be associated with osteoporosis. Variables that showed statistical significance in the univariate analysis, in addition to age, were then included in a multivariate logistic regression model to determine the independent predictors of osteoporosis. Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) software, Version 23, for Windows, and GraphPad Prism 6 software (Graph software, San Diego, CA). A P value < 0.05 was considered to indicate statistical significance.

Results

Demographic, clinical, and treatment characteristics

This study enrolled 130 individuals with LN, consisting of 2 males and 128 females. Among the female participants, 61 were premenopausal, and 67 were postmenopausal. Demographic characteristics, clinical profiles, and medication details of the patients are summarized in Table 1. Compared to premenopausal patients, postmenopausal patients exhibited several significant differences, including advanced age, later age at LN diagnosis, higher weight, lower height, elevated BMI, higher blood urea nitrogen level, and a more frequent use of bisphosphonate use (all P < 0.05).

Table 1 Demographics and clinical characteristics of premenopausal and postmenopausal LN patients
Full size table

BMD and prevalence of osteoporosis

The BMD measurements and the prevalence of osteoporosis across various skeletal sites are shown in Table 2. Compared to premenopausal patients, postmenopausal patients demonstrated significantly reduced BMD in the lumbar spine (L1-L4) (0.802 ± 0.165 vs. 0.877 ± 0.151 g/cm2, P = 0.008) and total hip (0.760 ± 0.143 vs. 0.814 ± 0.125 g/cm2, P = 0.027), and had lower T score at lumbar spine (L1-L4) (-2.194 ± 1.434 vs. -1.372 ± 1.403, P = 0.002), femoral neck (-1.576 ± 1.240 vs. -1.160 ± 1.052, P = 0.047), and total hip (-1.491 ± 1.167 vs. -1.079 ± 1.037, P = 0.041).

Table 2 Bone mineral density, T scores, and Z scores at different skeletal sites in all, premenopausal, and postmenopausal LN patients
Full size table

A significantly higher prevalence of osteoporosis at the spine (L1-L4) (50.7% vs. 19.7%, P < 0.001), femoral neck (29.9% vs. 4.9%, P < 0.001), total hip (25.4% vs. 6.6%, P = 0.009), and at least one measured site (55.2% vs. 24.6%, P < 0.001) was observed in postmenopausal patients compared to premenopausal patients.

Correlation of BMD with clinical characteristics

The spearman rank correlation coefficients between BMD and various demographics and clinical characteristics were given in Table 3. Notably, age at menopause, weight, height, and body mass index might be positively correlated with BMD in lumbar spine, total hip, and/or femoral neck. Conversely, age, age at diagnosis of LN, and menopause duration might be negatively correlated with BMD in these skeletal regions.

Table 3 Spearman rank correlation of BMD with demographics and clinical characteristics
Full size table

Further analysis using multivariable linear regression (Table 4) indicated that body mass index was positively associated with BMD; both disease duration and menopause duration were negatively associated with BMD of lumbar spine, total hip, and femoral neck in all and postmenopausal patients.

Table 4 Multivariate linear regression analysis for BMD in premenopausal and postmenopausal patients with LN
Full size table

Risk factors for osteoporosis

In the univariate logistic regression analysis for osteoporosis (Table 5), older age, older age at diagnosis of LN, younger age at menopause, lower weight, shorter height, and absence of bisphosphonates were identified as potential risk factors in LN patients. Specifically, in premenopausal patients, shorter height emerged as a potential risk factor for osteoporosis, while in postmenopausal patients, younger age at menopause, lower weight, shorter height, lower body mass index, and absence of bisphosphonates might be risk factors for osteoporosis.

Table 5 Univariate logistic regression analysis for osteoporosis in premenopausal and postmenopausal patients with LN
Full size table

In the multivariate logistic regression analysis (Table 6), we found that older age, lower weight, and absence of bisphosphonates were independently associated with an increased risk of osteoporosis in patients with LN. In premenopausal patients, lower height was independently associated with an increased risk of osteoporosis. In postmenopausal patients, younger age at menopause, lower weight, and absence of bisphosphonates were independently associated with an increased risk of osteoporosis.

Table 6 Multivariate logistic regression analysis for osteoporosis in premenopausal and postmenopausal patients with LN
Full size table

Discussion

In our investigation of Chinese patients with LN, we observed that 40% of the participants had osteoporosis. Furthermore, patients with SLE demonstrated a higher prevalence of reduced BMD compared that observed in the general Chinese population [23] and among Caucasian women with SLE [8]. In addition, the BMD values in our postmenopausal patients were slightly lower than those previously reported for the postmenopausal SLE population in Hong Kong [14].

Notably, our study found that the lumbar spine had a higher prevalence of osteoporosis in patients with LN. This finding aligns with previous research indicating a high risk of fracture in the lumbar spine for patients with SLE [7, 24]. Considering the potential consequences of lumbar spine issues, it is crucial to prioritize the bone health in LN patients. This involves ensuring adequate attention, conducting timely examinations, and implementing effective treatment strategies to mitigate the risk of osteoporosis and other related complications.

The etiology of bone loss in SLE is complex and multifaceted, influenced by a variety of factors including advanced age, postmenopausal status, low body mass index, disease-related elements, and medication-related side effects [8, 25,26,27,28,29]. Our research revealed a higher prevalence of osteoporosis in postmenopausal patients with LN compared to premenopausal patients (55.2% vs. 24.6%). Importantly, early menopause, defined as menopause occurring before the age of 45 [30], was observed in 21 out of 67 postmenopausal patients in our study. This could be attributed to the SLE disease itself or its treatment involving cytotoxic agents [31, 32]. Menopause is a well-established risk factor for bone loss because of decline in sex hormone levels, which play a critical role in regulating bone metabolism [33]. Therefore, it is necessary to emphasize the bone health in postmenopausal patients with LN.

Our study also found that lower body weight was associated with an increased risk of osteoporosis in the overall LN patient population, with similar findings in the postmenopausal subgroup. Involuntary weight loss, a common occurrence in LN [34], can adversely affect overall health. Previous studies have demonstrated that weight loss is associated with reduced BMD [35, 36], and an elevated risk of fractures [37]. Conversely, weight gain can positively affect bone maintenance by increasing the load on bones. In addition, higher body weight is linked to increased production of hormones like estrogen and testosterone, which are vital for bone maintenance [38]. Obese women have always been considered protected against osteoporosis and osteoporotic fractures [39]. However, postmenopausal women undergo significant hormonal shifts, including a decline in estrogen levels and a rise in circulating androgens [40]. These fluctuations render postmenopausal women more susceptible to alterations in body composition, such as muscle wasting and the accumulation of visceral fat [40,41,42,43]. The relative effect of fat mass on BMD still remains controversial [44]. Cui et al. observed that in postmenopausal women fat mass was positively associated with BMD at all sites, whereas both lean mass and fat mass contributed to hip BMD [45]. A recent study reported that, in postmenopausal women, fat mass was positively associated with BMD, but with relevant difference according to the differing skeletal sites [46]. The protective effect of BMI against hip fractures appears to have an element that is separate from BMD, likely attributed to the cushioning effect of adipose tissue around the greater trochanter [39]. However, excessive body fat, and particularly abdominal fat, produces inflammatory cytokines which may stimulate bone resorption and reduce bone strength [44]. Therefore, the impact of body weight, especially fat mass, on BMD may still be controversial and requires confirmation from future studies with larger samples and better design.

Our research found that the absence of bisphosphonates use may be associated with an increased risk of osteoporosis, with the following possible mechanisms. Firstly, the molecular structure of bisphosphonates, characterized by a P-C-P structure where carbon atom replaces the central oxygen atom in pyrophosphate, enables stable binding to bone hydroxyapatite. This binding ability is the foundation of the efficacy of bisphosphonates. Secondly, the potency of bisphosphonates is significantly influenced by the structures of their two side chains, R1 and R2. Notably, the presence of nitrogen atoms in the R2 side chain, a characteristic feature of second-generation bisphosphonates, markedly amplifies their potency. Thirdly, bisphosphonates mainly exert their effect by modulating osteoclast activity and lifespan; they diminish the number of active osteoclasts by inhibiting their recruitment and by suppressing osteoclast-activating signals from osteoblasts. Collectively, these mechanisms work together to help reduce bone loss, thereby reducing the risk of osteoporosis. In our study, we observed that postmenopausal LN patients exhibited a higher proportion of bisphosphonate usa compared to premenopausal patients (59.7% vs. 24.6%, P < 0.001). Both univariate (OR = 0.301, 95% CI 0.145–0.627) and multivariate (adjusted OR = 0.379, 95% CI 0.171–0.841) logistic regression analyses indicated a protective association between using bisphosphonate use and a reduced risk of osteoporosis. Bisphosphonate therapy appears to be beneficial in managing osteoporosis in LN patients. However, despite the usage rate being more than twice as high in postmenopausal patients compared to premenopausal patients, it may still be inadequate. Additional risk factors, such as early menopause and low body weight, could be influencing the postmenopausal population.

Our study did not reveal a significant association between the use of glucocorticoids and bone loss in LN patients. Given that glucocorticoids are a cornerstone of LN therapy [47,48,49], with nearly all of our study participants (97.8%) having been treated with them, it was not feasible to assess the relationship between the glucocorticoid exposure and the osteoporosis. Moreover, our study did not evaluate the cumulative dose of glucocorticoid administered. Due to these limitations, our study cannot determine the impact of glucocorticoid use on bone mass. Furthermore, adequate measures were taken to protect against osteoporosis in the patients we included, with 87.9% receiving calcium supplementation, 35.2% receiving α-calcitriol/calcitriol, and 53.8% receiving bisphosphonates. These protective interventions could potentially interfere with the assessment of the impact of glucocorticoids on osteoporosis. Further studies should incorporate more detailed data and a larger sample size are needed to assess the influence of glucocorticoids on bone mass.

We acknowledge certain limitations in our study. First, the inclusion of patients with LN at various disease durations for BMD measurements could introduce potential variability in the results. It is important to consider the potential influence of disease duration on BMD values. Second, the wide variation in treatments received by patients may introduce confounding factors that could impact the association between risk factors and osteoporosis. Third, previously known important factors that might be associated with osteoporosis, including cumulative doses of glucocorticoid use and serum levels of vitamin D, parathormone, alkaline, were not been evaluated and adjusted. Fourth, the patients included in our study were diagnosed by renal biopsy, and the vast majority of them had good renal function, which may not represent all LN patients.

Conclusion

Our findings indicate that patients with LN are at significant risk of developing osteoporosis, particularly in the lumbar spine and among postmenopausal individuals. The risk factors associated with osteoporosis that were identified may include older age, lower weight, and the absence of bisphosphonate treatment.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

The authors greatly appreciate all the hospital staff for their efforts in recruiting and treating patients and thank all patients involved in this study.

Funding

This work was financially supported by the National Natural Science Foundation of China under Grant Nos. [82170701 and 81974087], the 2019 Wuhan Yellow Crane Talents Program (outstanding young talents) and the Scientific Research Fund Project of Tongji Hospital (2021B17).

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  1. Yi Yang and Ying Yao were equal contributors.

Authors and Affiliations

  1. Department of Nephrology, Tongji hospital affiliated to Tongji medical college, Huazhong University of Science and Technology, Wuhan, Hubei, China

    Yu Hong, Yi Yang & Ying Yao

  2. Department of Nutrition, Tongji hospital affiliated to Tongji medical college, Huazhong University of Science and Technology, Wuhan, Hubei, China

    Ying Yao

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YH: software, data analysis, and writing—original draft. Yi Yang: writing—original draft, formal analysis, funding acquisition and methodology. Yi Yang: conceptualization, funding acquisition, and writing—reviewing and editing. All authors contributed to the article and approved the submitted version.

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Correspondence to Yi Yang.

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Ethics approval and consent to participate

The study protocol was approved by the Ethical Committee of Tongji Hospital Affiliated to Tongji Medical College, Huazhong University of Science and Technology (Project No. TJ-IRB20181106). This study was conducted in accordance with the ethical guidelines of the Declaration of Helsinki and informed consent was obtained from each patient.

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The authors declare no competing interests.

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Hong, Y., Yang, Y. & Yao, Y. Prevalence and risk factors of osteoporosis in lupus nephritis patients in China: a cross-sectional study. BMC Nephrol 25, 428 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12882-024-03882-7

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12882-024-03882-7

Keywords

BMC Nephrology

ISSN: 1471-2369

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