Association of the correlation between age-related renal failure and osteoporosis based on trabecular bone score in Bushehr Elderly Health (BEH) program

doi:10.21203/rs.3.rs-2217032/v1

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Research Article

Association of the correlation between age-related renal failure and osteoporosis based on trabecular bone score in Bushehr Elderly Health (BEH) program

https://doi.org/10.21203/rs.3.rs-2217032/v1

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Journal Publication

published 28 Jul, 2023

Read the published version in BMC Nephrology →

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Purpose

Osteoporosis is a systemic disease characterized by decreased strength of bone and increased risk of fracture in old age. Age and pathologic renal failure are independent risk factors for osteoporosis. However, it is not determined whether age related decreased renal function in the context of senescence can be considered as an independent risk factor for osteoporosis. Therefore, this study conducted to evaluate the effect of senescence induced renal failure on bone quality and trabecular bone score.

Methods

Using a cross-sectional design, this study was carried out based on data collected during BEH program on phase II. 2125 elderly participants aged more than 60 years old entered the study after fulfilling inclusion criteria and obtaining informed consent. They were examined for weight, height, abdominal and hip circumference and blood pressure measurement. All participants underwent DXA to assess bone mass density (BMD). Trabecular bone score (TBS) calculated using DXA apparatus software output. Univariate and adjusted multivariate linear regression were used to evaluate the associations.

Results

In univariate linear regression analysis there was a direct correlation between age-related renal failure and TBS (β = 0.038 and P = < 0.0001), neck of femur BMD (β = 0.047, P < 0.0001), lumbar BMD (β = 0.055, P < 0.0001) but after adjusting to BMI, age, sex, smoking and physical activity, there was not shown significant association for these variables.

Conclusion

It is hypothesized that in elderly aged more than 60 years old, age-related renal failure cannot be considered as an independent risk factor for osteoporosis.

osteoporosis

age-related renal failure

trabecular bone score

Elderly

In the recent years there is a sizable increase in geriatrics population following the increase in life expectancy and average of life span. This population has individualized age-related medical problems like osteoporosis. Osteoporosis which is the leading cause of minimal trauma fractures in elderly people is defined as reduced bone strength and density of 2.5 standard deviation below that of young adult(1). A number of etiologies have been introduced as proven risk factors of osteoporosis in the elderly such as female gender, smoking, alcohol consumption and some medical disease such as chronic kidney disease which is a major risk factor for fracture and decreased bone mineral density in the hip (2).

Although the previous studies confirmed the association of reduced kidney function with decreased BMD and bone loss(3, 4), it is not cleared whether senescence related decline in renal function in the absence of other well-known etiologies of renal failure, can have similar effects on BMD and bone loss.

Kidney like other organs undergoes some physiologic and structural alterations in the aging process which are not distinguishable to other secondary causes of structural and physiologic changes(5). There are some evidences imply on the possible association of age-related physiologic alterations in the kidney with decreased BMD. During kidney senescence, decreased activity of renal 1α-hydroxylase together with diminished absorptive ability of calcium in the intestine, result in secondary hyperparathyroidism and bone loss(6). Moreover, senescence results in decreased expression of vitamin D receptor and Transient Receptor Potential cation channel subfamily V 5 (TRPV5) in the kidney, leading to lower calcium reabsorption in renal tubules (7).

Although, the available physiologic evidences may predict the possible association between age-related decreased renal function as an independent risk factor with bone loss, there are some other contradictory reports about this association. Therefore, this study conducted to investigate the association between age-related decline in renal function with BMD and bone quality, based on the trabecular bone score with considering the effect of other factors in elderly population of BEH program.

Study population

The protocols of this study for phase one and two of BEH program were published previously(8, 9). Using a cross-sectional design, this study conducted based on data obtained during Bushehr Elderly Health Program (BEH). BEH program is an ongoing prospective population-based cohort study performed on a sample of elderly ≥ 60 years in urban population of Bushehr city, the center of Bushehr province located in the north part of Persian Gulf to determine the prevalence and risk factor of non-communicable disease (NCD).

Data Collection

Data such as demographic, physical activity, and smoking consumption were collected by trained interviewers. Demographic and life style data collected using standard self-reported questionnaire (6, 7). For physical activity the Global Physical Activity Questionnaire (OPAG), and a brief Tobacco Questionnaire were used for data collection. Tobacco smoking consumption were defining into three categories. First nonsmoker which means have not any experience of hookah or cigarettes consumption, past smoker was defined as any kind of consumption of tobacco smoking include (cigarettes or hookah) in the past but not used at the time of the study, and third current smoking defined as current smoking of either cigarette or hookah consumption, regularly or occasionally.

The physical activity level in 24 h of work, spots, and leisure time was calculated baes on metabolic equivalent. Lifestyle was classified based on five categories. No active which means have not any activity. Sedentary: 1-1.39, low active :1.4–1.59, active :1.6–1.89, very active :1.9–2.5)(10).

Anthropometric indexes including height, weight, were measured based on the NHANSE III anthropometric measurement protocol and Body mass index (BMI) was calculated using the formula weight (kg)/ [height (m)]² (11).

Medical Examination

Medical examination was done by physicians, and then registered in a file assigned to each of people accompanying the data from their laboratory test(12).

Fasting blood samples were taken following 8–12 hour overnight fasting. Fasting plasma glucose (FPG), calcium (Ca), phosphorus (P), Uric Acid and creatinine (Cr) were measured by an auto-analyzer using commercial kits (Pars Azmoon, Karaj, Iran).

The femoral neck, total hip and lumbar spine (L1-L4) BMD were measured using DXA (Hologic Inc., USA) and the TBS iNsight ® software was installed on the DXA machine to calculate L1-L4 TBS.

Definitions

Estimated Glomerular Filtration Rate

(eGFR) was calculated using modified of diet in renal disease (MDRD) formula based on plasma creatinine.

175×(Cr)^−1.154× (age)^−0.203×0.742 (if a woman) ×1.210 (if black race)(13).

Inclusion & Exclusion Criteria

In summary the inclusion crtiteria were define as individual more than sixty years of age, residence of Bushehr city at least one years before involve in the study. Participants should not have any future plan for movement or leaving the city, have enough ability to taking part in the program, also each people should complete the informed consent. The male and female subjects were excluded if they had serum Cr ≥ 1.3 and 1.1 respectively or had positive history of diabetes mellitus or uncontrolled hypertension.

Ethical Considerations

The study approval was done by the Ethical Research Committee (ERC) of Endocrinology and Metabolism Research Institute affiliated, and ERC of Bushehr University of Medical Sciences. Informed consent was obtained from all participants. (Ethical Code: IR.TUMS.EMRI.REC.1394.0036)

Statistical Analysis

The Normal distribution of continuous variables was checked using the Kolmogrove-Smirnov test. For continuous variables the mean and standard deviation were used to illustrate the descriptive statistics. For qualitative data the number and percentage were used. The P-value less than 0.05 defined as significance. For assessing the difference between definition of osteoporosis (based on BMD, and TBS) and GFR status (between 45–60, and more than 60) univariate and multivariate linear regression model were used. In the multivariate analysis three models were used. In the first model (age and sex), the second model (age, sex, physical activity, and current smoker), and the final model (age, sex, physical activity, and current smoker, BMI) were used for adjusting the models. The criteria for selecting the variables were based on the P value less than 0.05 in the univariate model based and clinical implication based on the literatures. All analyses were performed using STATA (Release 12, Statistical software. College Station, Texas: STATA Corp LP).

The mean age of the participants was 68.83 ± 6.04 years, which 54.44% were female. Among the total participants, 405 (21.66%) of them were using current cigarette or hookah, however; 897 (47.97%) of participant were reported past consumption of tobacco. Only about 7% of the elderly people were active, the other participants had sedentary life, low active or without activity. General characteristics of the participants according to their GFR status are illustrated in Table 1. (Table 1)

Table 1

General characteristics of the participants based on their GFR status
		Total	GFR = 45–60	GFR > 60
		Mean ± SD	Mean ± SD	Mean ± SD
BMI		27.42 ± 4.79	28.24 ± 5.08	27.28 ± 4.73
Age		68.83 ± 6.04	71.2 ± 7.13	68.41 ± 5.71
Calcium		9.35 ± 0.52	9.46 ± 0.54	9.33 ± 0.51
Phosphor		4.01 ± 0.55	4.11 ± 0.50	3.99 ± 0.56
Uric Acid		4.91 ± 1.10	5.17 ± 1.02	4.87 ± 1.11
Sex		N (%)	N (%)	N (%)
	Female	1,018 (54.44%)	227 (79.65%)	789 (50.00%)
	Male	852 (45.56%)	58 (20.35%)	789 (50.00%)
smoking	None	568 (30.37%)	85 (29.82%)	481 (30.48%)
	Past-cigarette or hookah	897 (47.97%)	137 (48.07%)	757 (47.97%)
	current cigarette or hookah	405 (21.66%)	63 (22.11%)	340 (21.55%)
Physical activity	< 1 = NO activity	104 (5.56%)	32 (11.23%)	72 (4.56%)
	1-1.39 = Sedentary	1,313 (70.21%)	189 (66.32%)	1121 (71.04%)
	1.4–1.59 = Low active	325 (17.38%)	43 (15.09%)	279 (17.68%)
	1.6–1.89 = Active	107 (5.72%)	20 (7.02%)	86 (5.45%)
	>=1.9 = Very active	21 (1.12%)	1 (0.35%)	20 (1.27%)

As it is demonstrated in Table 2, neck of femur BMD, lumbar BMD, and the L1-L4 TBS were significantly higher in GFR > 60 compare to the GFR 45–60. (Table 2).

Table 2

Bone health status of the individual based on their MDRD status
	GFR = 45–60	GFR > 60	P-value
Neck of femur BMD mean (SD) gr/cm²	0.614 ± 0.134	0.661 ± 0.141	< 0.0001
Lumbar BMD mean (SD) gr/cm²	0.838 ± 0.160	0.893 ± 0.180	< 0.0001
TBS (L1-L4) mean (SD)	1.259 ± 0.102	1.298 ± 0.103	< 0.0001

Univariate linear regression results revealed that GFR more than 60 had a significant, and positive association with Neck of femur BMD (β = 0.047, P < 0.0001). But the association was not significant in multivariable regression model after adjusting for age, sex (β = -0.015, and P = 0.052). Moreover, univariate linear regression results revealed a significant positive association between GFR > 60 with lumbar BMD (β = 0.055, P < 0.0001) while this association was not significant after adjusting for age, sex (β =-0.009 and P = 0.358). The TBS L1-L4 also shows significant association in univariate model (β 0.038 and P = < 0.0001) but it was not significant after adjusting for age and sex (β =-0.002 and P = 0.718) and in the fully adjusted model (after adjustment for age, sex, physical activity, and current smoker, BMI) the beta decrease to the lowest level (β =-0.003 (-0.015–0.007). (Table 3)

Table 3

Linear association between TBS, BMD with MDRD status
	Neck of femur BMD mean		Lumbar BMD mean		TBS (L1-L4) mean (SD)
Univariate Model	Beta (95% CI)	P-Value	Beta (95% CI)	P-Value	Beta (95% CI)	P-Value
GFR = 45–60	Reference	Reference	Reference	Reference	Reference	Reference
GFR > 60	0.047 (0.029–0.064)	< 0.0001	0.055 (0.032–0.077)	< 0.0001	0.038 (0.025–0.052)	< 0.0001
*First Multivariate Model
GFR = 45–60	Reference	Reference	Reference	Reference	Reference	Reference
GFR > 60	-0.015(-0.030–0.0001)	0.052	-0.009 (-0.029–0.010)	0.358	-0.002 (-0.013–0.009)	0.718
**second Multivariate Model
GFR = 45–60	Reference	Reference	Reference	Reference	Reference	Reference
GFR > 60	-0.014 (-0.029–0.001)	0.072	-0.007 (-0.028–0.012)	0.464	-0.001 (-0.013- 0.009)	0.750
**Final Multivariate Model
GFR = 45–60	Reference	Reference	Reference	Reference	Reference	Reference
GFR > 60	-0.010 (-0.025–0.004)	0.172	-0.001 (-0.020–0.017)	0.860	-0.003 (-0.015–0.007)	0.533
Adjusted for age and sex Adjusted for age, sex, physical activity, and current smoker **Adjusted for age, sex, physical activity, and current smoker, BMI

Based on our knowledge this is the first community-based cross-sectional study, that evaluate the association between TBS and renal function status evaluated in elderly Iranian population. The mean values of femoral neck and lumbar BMD and TBS L1-L4 were significantly higher in participants with GFR > 60 compare to the GFR 45–60. Univariate linear regression results revealed a positive significant association between neck of femur BMD, lumbar BMD, and L1-L4 TBS with higher GFR. But in multivariate analysis, the associations between mentioned variables were not significant after adjusting fully model with age, sex, physical activity, smoking status and BMI.

Cumulating evidences confirmed the association between chronic kidney disease with osteoporosis and increased risk of fracture(14, 15). This association may apart be related to pathophysiologic alterations in chronic kidney disease such as secondary hyperparathyroidism, altered metabolism of active form of vitamin D, phosphorus retention, chronic metabolic acidosis, increased level of sclerostin and FGF23. These factors have pivotal role in the metabolism of bone minerals(16) .Therefore, it can be hypothesized that age related decline in renal function may result in decreased BMD in healthy elderlies. According to the results of current study this hypothesis has been failed to be confirmed.

Li et al, revealed a positive association between decreased renal function and lower BMD in postmenopausal healthy women with GFR > 60. But the adjusted model based on age, duration of menopause and BMI, failed to reveal significant association (11). The other cohort study signified the association of GFR and BMD in average age of 75 year old while in average age of 80 and 85 the association was not significant (3)

The majority of studies which indicated the association of renal failure with decreased BMD had been conducted on patients suffering from chronic kidney disease (17). Moreover, pathophysiologic alterations in renal failure leading to disturbance in bone mineral metabolism, almost invariably occurring in GFR < 60 which are not easily distinguishable from primary osteoporosis. The previous results about the effects of pathologic CKD on BMD may not be easily attributable to bone metabolism in age related renal failure in healthy elderlies. Therefore in extreme of age, according to the contrary results, other factors may modulate or even counteract the expected physiologic alteration of bone.

There are some well-known pathologic mechanisms involved in the pathogenesis of osteoporosis. It has been elucidated that Parathyroid hormone (PTH) had more increment in higher stages of renal failure .(17) Carrevick et al, revealed that in the extreme of age, PTH was still in high blood level irrelevant of GFR even in GFR more than 60 (18). In pathologic CKD models, it has been reported that PTH had not significant effect on bone metabolism in the extreme of GFR quartiles and there was an attenuated relationship between declined of GFR and fracture risk (19).Therefore, in healthy elderlies the altered PTH effect on bone may attenuate the strength of relationship between GFR and BMD.

FGF23 as an osteocyte-originated hormone and key regulator of phosphorous and vitamin D, has an important role in the pathogenesis of osteoporosis and TBS decline (20).This hormone which is started to be secreted in the GFR less than 60 (21)is inhibited by klotho. Moreover, klotho is increased in early stage of renal failure as a compensatory hormone (22). Therefore, in current study in the early stage of renal failure, the possible compensatory increase in klotho may decrease plasma level of FGF23, attenuate its destructive effect on TBS and modulate the effect of renal failure on TBS.

Receptor activator of nuclear factor-κB (RANK) pathway is a well-known pathway in the metabolism of bone minerals. The interaction between RANK and its ligand RANKL, results in stimulation of osteoclasts and production of cytokines (23). Osteoprotegrin (OPG) as an osteoblast derived anti-inflammatory protein inhibits osteoclasts through competitive inhibition of RANK and results in decreased bone resorption (24). The RANKL-OPG imbalance plays a major role in the pathogenesis of osteoporosis and inflammatory process (25). Therefore, OPG has been introduced as an anti-osteoporotic agent (26). It has been demonstrated that OPG increases with aging (27)and there is a GFR-independent positive correlation between OPG and aging. Vik et al, revealed a significant negative correlation between GFR and OPG in average age older than 62.2 (28).Therefore, it might be hypothesized that increased OPG may have a protective anti-osteoporotic role in age-related declined renal function.

The major limitation of this study was lack of measuring the parameters which are involved in the pathogenesis of osteoporosis such as PTH, FGF23, OPG, RANK and RANKL. The contradictory results of current study, necessitates further studies to clarify the exact mechanism of bone metabolism in the extreme of age. It can be hypothesized that the well-known pathophysiologic mechanisms responsible for pathologic CKD-induced osteoporosis may not exactly act in similar patterns in senescence induced renal failure in healthy elderlies. The physiologic alterations in the extreme of age may have unknown protective or stimulatory mechanisms performing through other unknown mechanism in bone mineral metabolism.

Osteoporosis is significant problem for the global community. With aging process the osteoporosis and related fracture that have a great impact in community, and burden of disease will likely continue to increase. Several early interventions are predicted for decline the mortality, morbidity, and economic impact of age-related osteoporosis. Although previous studies predict the effect of renal function as in independent risk factor for bone loss, however; the current study, when confounding variables are considered, it cannot indicate the direct and independent effect of renal dysfunction for osteoporosis. Future research is needed to determine the pathologic pathway of this hypothesis.

Acknowledgment:

The authors would like to express their appreciation to all medical research center employees at Bushehr University of Medical Sciences (BUMS) and Tehran University of Medical Sciences (TUMS) for their dedication and collaboration. The authors would also like to convey their heartfelt appreciation to the Persian Gulf Martyrs Hospital’s Clinical Research Development Center, the Persian Gulf Tropical Medicine Research Center, and Bushehr University Of Medical Sciences’s Student Research Committee. We would like to thank all participants for their participation in the study.

Funding:

The Persian gulf Biomedical Sciences Research Institute, affiliated with the Bushehr university of Medical Sciences (BPUMS) , and the Endocrinology and Metabolism Research Institute, affiliated with Tehran University of Medical Sciences, both contributed to funding for the BEH Program. This study project was designed and carried out with the help of researchers from both research institutions.

Availability of data and materials:

The datasets used during the current study are available from the corresponding author, AO ([email protected]) or IN ([email protected]) upon reasonable request.

Ethics approval and consent to participate:

The Declaration of Helsinki and Iranian national norms for research ethics are being followed in the conduct of this study. On September 23, 2013, The study was approved by the Ethics Committee of Bushehr University of Medical Sciences (ref. No. B-91–14-2). Informed consent was obtained from all study participants. The study's participants have the right to leave at any moment and without giving a reason. Data collected are stored in a re-identifiable form by national ID code. The results will be presented at national and international meetings and published in a peer-reviewed journal. We aim to translate the key findings into an easily understandable format for local residents and present them through local media. Relevant findings will also be presented as policy briefs to national and local health policymakers.

Competing interests:

The authors declare no conflict of interest

Consent for publication:

Not applicable.

Author contribution:

MM, AO conceived the study and performed data analysis and interpretation. MeM, AA, NH, and SNB drafted the manuscript and participated in interpretation, study design, and conduct and helped draft the manuscript and interpretation. IN, BL, MM, MeM, MKH and AO participated in the study design and interpretation of the findings. All authors reviewed and approved the submitted manuscript.

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No competing interests reported.

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You are reading this latest preprint version

Association of the correlation between age-related renal failure and osteoporosis based on trabecular bone score in Bushehr Elderly Health (BEH) program

Status:

Journal Publication

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Introduction

Material And Method

Study population

Data Collection

Medical Examination

Definitions

Estimated Glomerular Filtration Rate

Inclusion & Exclusion Criteria

Ethical Considerations

Statistical Analysis

Result

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1