Prevalence and Risk Factors of Osteosarcopenia in Elderly Patients with Type 2 Diabetes

doi:10.21203/rs.3.rs-4538577/v1

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Research Article

Prevalence and Risk Factors of Osteosarcopenia in Elderly Patients with Type 2 Diabetes

https://doi.org/10.21203/rs.3.rs-4538577/v1

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Journal Publication

published 19 Aug, 2024

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Purpose

To assess the prevalence of osteosarcopenia (OS) in elderly patients with type 2 diabetes mellitus (T2DM) and explore the related risk factors for developing this condition.

Methods

This cross-sectional study enrolled hospitalized T2DM patients aged 60 years and older. Patients underwent assessments of total hip bone mineral density (BMD), grip strength, the Short Physical Performance Battery (SPPB), and body composition. Based on the 2019 Asian Working Group for Sarcopenia (AWGS) criteria, appendicular skeletal muscle mass (ASM), grip strength, and SPPB were measured to diagnose sarcopenia. BMD and T values of the lumbar spine and hip were measured using dual-energy X-ray absorptiometry (DXA). Osteosarcopenia was defined when both sarcopenia and osteoporosis criteria were met. Statistical analysis included binary logistic regression to identify significant risk factors.

Results

A total of 254 hospitalized T2DM patients (80 males and 174 females) were included. They were divided into T2DM-OS (n = 58) and T2DM-NOS (n = 196) groups based on the presence of osteosarcopenia. The average ages were 72.724 ± 6.463 and 69.265 ± 6.035 years, respectively. The prevalence of osteosarcopenia in T2DM patients was 22.8%, with 20.7% (12 males) and 79.3% (46 females) in the T2DM-OS group. After adjusting for confounding factors, it was found that male gender (OR: 5.738, 95%CI: 1.602–20.551, P = 0.007), fasting plasma glucose (OR: 0.904, 95%CI: 0.821–0.995, P = 0.038), and ASMI (OR: 0.049, 95%CI: 0.013–0.184, P < 0.001) were major influencing factors for the development of osteosarcopenia in elderly T2DM patients.

Conclusions

The prevalence of T2DM-OS is relatively high, with male gender, low fasting plasma glucose, and low ASMI identified as risk factors.

type 2 diabetes mellitus

elderly

osteosarcopenia

risk factors

The increasing aging population globally, and specifically in China, has become a major public health concern. According to the 2023 National Statistical Yearbook[1], by the end of 2022, China's population aged 65 and above had reached 297 million, accounting for about 14.9% of the total population. This demographic shift has led to a rise in age-related health issues, particularly musculoskeletal diseases such as osteoporosis (OP) and sarcopenia (SP).

Osteoporosis, characterized by reduced bone density and increased fracture risk, and sarcopenia, defined by loss of muscle mass and strength, are common conditions among the elderly. Research indicates a positive correlation between the prevalence of sarcopenia and osteoporosis[2]. When these conditions coexist, known as osteosarcopenia(OS), the risks of frailty, falls, fractures, and disability significantly increase[3]. This synergistic effect highlights the importance of a comprehensive approach to musculoskeletal health, advocating for ‘muscle-bone co-treatment and prevention.’

Type 2 Diabetes Mellitus (T2DM) further complicates the health landscape for the elderly. T2DM is associated with poor bone strength and muscle atrophy[4]. Studies report that the global prevalence of diabetic sarcopenia reached 18% in 2020[5]. Elderly T2DM patients with sarcopenia exhibit higher rates of complications in target organs such as kidneys, feet, and peripheral nerves, alongside diminished daily activity capabilities, grip strength, and walking speed (54.2% vs. 35.5% when compared to non-sarcopenic patients)[6]. However, the impact of diabetes on osteosarcopenia remains under-researched, and the prevalence of osteosarcopenia in T2DM patients is not well documented.

This study aims to investigate the prevalence of osteosarcopenia among elderly T2DM patients in Longquanyi District, Chengdu. By identifying risk factors for its development, the study seeks to provide valuable references for secondary prevention and early intervention strategies in T2DM patients.

Study Subjects

This study was approved by the Academic Ethics Committee of the First People's Hospital of Longquanyi District, Chengdu (Ethics Approval No.AF-KY-202210). We consecutively enrolled elderly hospitalized patients with T2DM from June 2023 to January 2024. The inclusion criteria were: age ≥ 60 years; meeting the 1999 World Health Organization (WHO) diagnostic criteria for diabetes; and providing informed consent to participate in the study and willingness to participate in the survey. Exclusion criteria included: patients with mental disorders; a history of paralysis or Parkinson's disease; cognitive or communication impairments that prevent cooperation with the examination; implanted metal devices such as pacemakers, artificial joints, or intrauterine devices, which may affect the accuracy of body composition tests; acute infectious diseases or chronic wasting diseases such as tuberculosis, malignant tumors, or HIV infection; and severe chronic gastrointestinal diseases.

The sample size was estimated using the formula for cross-sectional study sample size calculation: 𝑁 =t_α^༒PQ/d^༒. Here, 𝑁 is the estimated sample size, P is the population rate, determined to be 15.1% based on a study on sarco-osteoporosis among elderly community-dwelling residents in China[7]. With a significance level 𝛼 of 0.05, the statistical value t_α=1.96,Q = 1-P, and an allowable error 𝑑 of 0.05, the calculated sample size 𝑁≈197. Considering a 10% sample attrition rate, the minimum sample size was determined to be 219. The final sample size of this study was 254, which met the sample size requirement.

Collection of General Patient Information and Clinical Indicators

General information collected included patient age, gender, height, weight, and BMI. Clinical indicators encompassed fasting plasma glucose (FPG), glycated hemoglobin (HbA1C%), bone mineral density (BMD) and T-scores of the lumbar spine, femoral neck, and total hip, handgrip strength, time to complete five chair stands, appendicular skeletal muscle mass (ASM), Short Physical Performance Battery (SPPB) scores, body composition metrics, Activities of Daily Living (ADL) scores, and fall risk assessments.

Definition and Measurement of Osteoporosis

Osteoporosis was assessed using a dual-energy X-ray absorptiometry (DXA) scanner (Lunar iDXA) to measure the BMD and T-scores of the lumbar spine and hip. According to the Guidelines for the Diagnosis and Treatment of Primary Osteoporosis (2022)[8], osteoporosis is diagnosed in men aged 50 and older or postmenopausal women if they have a T-score ≤ -2.5 at any site (lumbar spine or hip) or a history of fragility fractures.

Definition and Measurement of Sarcopenia

According to the 2019 consensus by the AWGS, sarcopenia is defined based on muscle mass, muscle strength, and physical performance. Possible sarcopenia is indicated by decreased muscle strength and/or physical performance. Sarcopenia is diagnosed when there is reduced skeletal muscle mass along with either decreased muscle strength or physical performance. Severe sarcopenia is identified when all three conditions are present.

Muscle Mass: Measured using the InBody S10 body composition analyzer through bioelectrical impedance analysis (BIA). Muscle mass is assessed using the Appendicular Skeletal Muscle Mass Index (ASMI), calculated as limb skeletal muscle mass (kg) divided by height squared (m²), with thresholds of ≤ 7.0 for men and ≤ 5.7 for women.

Muscle Strength: Evaluated using a baseline hand dynamometer (CH43100) digital grip strength dynamometer. Grip strength is measured three times for each patient, with 15-second intervals between measurements, and the average value is recorded. Decreased muscle strength is defined as < 28 kg for men and < 18 kg for women.

Physical Performance: Assessed using the Short Physical Performance Battery (SPPB), introduced by Guralnik et al. in 1994. The SPPB includes three components: balance tests (side-by-side, semi-tandem, and tandem stands), gait speed test (4-meter walk), and chair stand test (time to complete five chair stands). Each component is scored from 0 to 4, with a total score ranging from 0 to 12. A total score of ≤ 9 indicates decreased physical performance.

Diagnosis of Osteosarcopenia

According to the Expert Consensus on Osteosarcopenia, osteosarcopenia is diagnosed when both the criteria for sarcopenia and osteoporosis are met simultaneously[9].

Statistical Analysis

Statistical analysis was performed using SPSS 25.0 software. Measurement data were described using mean ± standard deviation for normally distributed data, and group comparisons were conducted using the t-test. For non-normally distributed data, the median (upper quartile, lower quartile) was used for description, and group comparisons were performed using the Wilcoxon rank-sum test. Categorical data were described using frequencies and percentages, with group comparisons made using the χ² test or Fisher's exact test. The factors influencing osteosarcopenia in patients with type 2 diabetes were analyzed using binary logistic regression, presented with OR values, 95% CIs, and P-values, with a significance level set at P < 0.05.

Comparison of Clinical Characteristics Between T2DM-OS and T2DM-NOS

A total of 254 elderly patients with T2DM were included in this study. Among them, 58 patients were diagnosed with OS(T2DM-OS), resulting in a prevalence of 22.8%. This included 12 males (20.7%) and 46 females (79.3%). The clinical characteristics of the T2DM patients with OS were compared to those without OS, as shown in Table 1.

Single-Factor Analysis

The analysis reveals significant differences between the T2DM-OS and T2DM-NOS groups regarding gender, age, BMI, FPG, the SPPB score, grip strength, ASMI, upper arm circumference, body water content, bone mineral content, protein content, and the ADL score (P < 0.05). Conversely, no statistically significant differences were observed in body fat percentage, visceral fat area, HbA1C, and the MFS score (P > 0.05). Detailed information can be found in Table 1.

Table 1: Comparison of Clinical Characteristics Between T2DM-OS and T2DM-NOS

Items	T2DM-OS (n = 58)
Gender[n%]
Male	12(20.7)	68(34.7)	4.068^b	0.044
Female	46(79.3)	128(65.3)	4.068^b	0.044
Age( years )	72.724 ± 6.463	69.265 ± 6.035	3.773^a	0.000
60–74	37(63.8)	159(81.8)	7.628^b	0.006
≥ 75	21(36.2)	37(18.9)	7.628^b	0.006
BMI(Kg/m2)
< 18.5	4(6.9)	4(2.0)	16.574^b	0.001
18.5-23.99	34(58.6)	69(35.2)
24-27.99	18(31.0)	98(50.0)
≥ 28	2(3.4)	25(12.8)
FPG(mmol/L)	7.07(6.12,9.82)	9.08(6.41,12.29)	-2.350^c	0.019
HbA1C(%)	9.702 ± 2.810	9.771 ± 2.581	-0.175^a	0.861
SPPB(Scores)
0–6	12(20.7)	16(8.1)	12.376^b	0.002
7–9	33(56.9)	94(48.0)
10–12	13(22.4)	86(43.9)
Grip Strength (Kg)	14.232 ± 5.118	17.825 ± 7.878	-3.272^a	0.001
ASMI(Kg/m2)	5.331 ± 0.619	6.460 ± 0.799	-9.904^a	0.000
Upper arm circumference (cm)	27.05(25.40,29.22)	30.00(28.20,31.40)	-6.252^c	0.000
Total muscle mass (Kg)	16.924 ± 2.223	20.900 ± 3.560	-8.045^a	0.000
Body fat percentage (%)	35.20(31.00,39.80)	34.40(29.92,39.10)	-0.601^c	0.548
Body water content (L)	23.991 ± 2.806	28.892 ± 4.429	-7.962^a	0.000
Bone mineral content(Kg)	1.962 ± 0.180	2.213 ± 0.309	-5.886^a	0.000
Protein(Kg)	6.10(5.87,6.72)	7.40(6.80,8.40)	-7.712^c	0.000
Visceral fat area (cm2)	98.55(70.30,123.00)	101.70(82.00,130.30)	-1.407^c	0.159
ADL
Mild to Moderate Dependence	30(51.7)	63(32.1)	7.394^b	0.007
Completely Independent	28(48.3)	133(67.9)
MFS
Low	37(63.8)	128(65.3)	3.449^b	0.178
Medium	16(27.6)	62(31.6)
High	5(8.6)	6(3.1)

Abbreviations: BMI = body mass index, FPG = fasting plasma glucose, HbA1c = glycated hemoglobin, ADL = Activities of Daily Living, MFS = Morse Fall Scale

a' = t-test, 'b' = Chi-square test, 'c' = Z-test

Multifactorial Logistic Regression Analysis of Osteosarcopenia Occurrence in Elderly T2DM Patients

A multifactorial logistic regression analysis was performed to investigate the occurrence of osteosarcopenia in elderly T2DM patients, with the presence of osteosarcopenia as the dependent variable (No = 0, Yes = 1). Independent variables with significant differences in the univariate analysis were included: gender (Male = 1, Female = 2), age (60–74 years = 1, ≥ 75 years = 2), BMI (< 18.5 kg/m² = 1, 18.5-23.99 kg/m² = 2, 24-27.99 kg/m² = 3, ≥ 28 kg/m² = 4), SPPB total score (0–6 points = 1, 7–9 points = 2, 10–12 points = 3), and ADL score (mild to moderate dependence = 1, complete self-care = 2). The Box-Tidwell method was used to test the linear relationship between upper arm circumference and ASMI with the logit-transformed dependent variable, and multicollinearity was assessed using a linear model test. Due to collinearity between skeletal muscle mass and ASMI, ASMI was chosen for the logistic regression model. The model showed no significant difference between predicted and actual values of osteosarcopenia occurrence (P > 0.05), with good fit (Hosmer-Lemeshow test, P > 0.05) and an accuracy of 82.7%.

The results indicated that FPG, gender, and ASMI were the main influencing factors for osteosarcopenia in elderly T2DM patients (P < 0.05), as shown in Table 2. Higher FPG levels (B = -0.101, OR = 0.904, P = 0.038) were associated with a decreased likelihood of osteosarcopenia. Males (B = 1.747, OR = 5.738, P = 0.007) were significantly more likely to develop osteosarcopenia compared to females. Additionally, higher ASMI values (B = -3.011, OR = 0.049, P = 0.000) were linked to a lower risk of osteosarcopenia. These findings indicate that gender, FPG, and ASMI are crucial factors in predicting osteosarcopenia in this patient population.

High Prevalence of Osteosarcopenia in Elderly T2DM Patients

The prevalence of osteosarcopenia varies significantly across different countries and regions. Liu Keru et al.[10] conducted a study on the elderly community in Shihezi, Xinjiang, and reported an osteosarcopenia detection rate of 21.9%. This rate is higher than the 12.7% prevalence found in a 2015 study by Wang et al. in the elderly community of Changsha[7]. The increased incidence of osteosarcopenia in T2DM patients can be attributed to the detrimental effects of type 2 diabetes mellitus on bone and muscle health. Pechmann et al.'s research demonstrated that the prevalence of osteosarcopenia is significantly higher in T2DM patients compared to non-diabetic controls (11.9% vs. 2.14%, p = 0.010)[11]. In our study, the prevalence of osteosarcopenia in T2DM patients was found to be 22.8%, which is higher than previously reported figures.

Moretti et al. conducted a study on postmenopausal women and found a 50% prevalence of osteosarcopenia in those with T2DM, significantly higher than the 17% prevalence in the non-T2DM group (OR 5.0, 95% CI 1.05–23.79, p = 0.043)[4]. This rate is substantially higher than the findings of our study. The differences in prevalence rates across various studies may be due to variations in the study populations and the screening tools used. Despite these discrepancies, it is evident that the incidence of osteosarcopenia is considerably high among T2DM patients. Therefore, there is a pressing need to raise awareness about osteosarcopenia in diabetic patients and to implement early screening and intervention strategies to manage this condition effectively.

Male Gender as a Risk Factor for T2DM-OS

Previous research has indicated that endocrine metabolic dysfunctions, such as diabetes and lack of physical activity, significantly impact muscle and bone health[12]. Diabetic patients often exhibit lower cortical bone density, which leads to decreased bone mass and an increased risk of fractures[13]. Additionally, insulin resistance can accelerate muscle loss. Studies have established that men have a higher incidence of sarcopenia, while women are more prone to osteoporosis[14]. However, the gender differences in T2DM patients who simultaneously suffer from sarcopenia and osteoporosis remain underexplored. Our findings, as shown in Table 2, demonstrate that elderly male T2DM patients are significantly more likely to develop osteosarcopenia compared to female patients (OR = 5.738). This aligns with a study by Liu et al. (2017) conducted in China[15], which found that the prevalence of combined sarcopenia and osteoporosis in T2DM patients was significantly higher in men than in women (30.9% vs. 8.6%). Fahimfar et al. (2018) also reported that diabetic men are more susceptible to osteosarcopenia (PR = 1.33, 95% CI: 1.04–1.69) and highlighted a significant association between physical activity and osteosarcopenia in men, but not in women[16]. These findings are consistent with our results.

However, a study by Wang et al. (2020) reported no significant gender differences in the prevalence of osteosarcopenia, contradicting our findings[17]. This inconsistency might be due to variations in the study populations and the diagnostic criteria for sarcopenia. Differences in genetic, lifestyle, and environmental factors could also contribute to these variations.

Table 2

Multifactorial Logistic Regression Analysis of Osteosarcopenia Occurrence in Elderly T2DM Patients
Variables	B	SE	Wald	OR(95%CI)	P value
Constant	21.924	5.778	14.399	/	0.000
FPG	-0.101	0.049	4.291	0.904(0.821,0.995)	0.038
Gender (Male)	1.747	0.651	7.205	5.738(1.602,20.551)	0.007
ASMI(kg/m2)	-3.011	0.672	20.051	0.049(0.013,0.184)	0.000
Dependent variable: sarcopenia (1 = yes, 0 = no). Coding: gender (male = 0, female = 1); continuous variables in original values

Low FPG as a Risk Factor for T2DM-OS

Low FPG as a Risk Factor for Osteosarcopenia in T2DM Patients

Poor blood glucose control in diabetes and sarcopenia interacts with each other. Long-term hyperglycemia can lead to bone loss, decreased muscle mass, and function[18]. Sugimoto et al. showed that the prevalence of sarcopenia increased linearly with the increase of HbA1c concentration and FPG was negatively correlated with SMI[19]. Pechmann et al. showed that the presence of osteosarcopenia in T2DM patients was associated with chronic diabetic complications but not with increased FPG or HbA1c levels[11]. However, this study found that low FPG was a risk factor for osteosarcopenia in T2DM patients (OR = 0.904), which was inconsistent with the above research results. The reason for the analysis may be related to differences in the population included in the study and factors such as blood glucose fluctuations.

Blood glucose levels typically reach their lowest point in the early morning and before meals. In this study, the HbA1c concentrations of the two groups of T2DM patients were relatively high (greater than 9.7%). Under conditions of long-term high blood glucose levels, a reduction in FPG may indicate increased blood glucose fluctuations. According to Ogama et al.'s research, even after adjusting for HbA1c levels and other relevant factors, blood glucose fluctuations in T2DM patients were independently associated with sarcopenia[20]. Furthermore, this study did not find a correlation between HbA1c levels and osteosarcopenia in T2DM patients, which is inconsistent with the findings of Korean scholar Yoon et al.[21], who reported that when HbA1c exceeded 8.5%, muscle function declined, and the prevalence of sarcopenia significantly increased. This inconsistency might be due to the fact that there was no significant difference in HbA1c levels between the two groups of patients with and without osteosarcopenia in this study (t=-0.175, P > 0.05). Future research is needed to further investigate the impact of blood glucose levels (including FPG and HbA1c) on osteosarcopenia in T2DM patients.

High ASMI as a Protective Factor Against T2DM-OS

The skeletal muscle mass index is an important indicator for evaluating skeletal muscle mass. Muscle strength has been recognized as the best predictor of health outcomes in both diabetic and non-diabetic patients[22]. As age increases, SMI tends to decrease, with an average decline of 5.8% from the youngest to the oldest age group [23]. Considering that the study cohort spans approximately 20 years from the youngest to the oldest age group, the annual decline in skeletal muscle index is only 0.29%. Previous studies have indicated that muscle strength in diabetic patients is lower than in non-diabetic individuals[24], and T2DM is associated with accelerated loss of leg muscle strength in older adults[25]. Liu et al. demonstrated that SMI is independently associated with osteoporosis in prediabetic adults (OR 0.65, 95% CI 0.50–0.85)[26]. Currently, there is a lack of research on the relationship between SMI and osteosarcopenia in diabetic patients.

This study shows that as the SMI increases, the risk of osteosarcopenia in elderly T2DM patients decreases (OR = 0.049). This finding is consistent with the results of Intriago[27], who found that patients with osteosarcopenia had lower ASM, SMI, and total-body skeletal muscle mass compared to those with osteopenia/osteoporosis or normal individuals. Additionally, this study found that BMI has no significant impact on the occurrence of osteosarcopenia, which aligns with the findings of Zhao Yu et al.[28], who studied the correlation between sarcopenia diagnosed by CT and osteoporosis in elderly T2DM patients. This lack of significance may be due to BMI being influenced by abnormal fat distribution, making it an inaccurate reflection of osteosarcopenia characteristics.

Limitations

This study is a cross-sectional study, which limits the ability to establish a causal relationship between osteosarcopenia and related metabolic indicators in type 2 diabetes patients. Although adjustments were made for factors such as gender, age, and physical function in the statistical analysis, some important questionnaire items, such as dietary habits and exercise frequency, were not considered. Additionally, the study population was limited to Chinese patients with type 2 diabetes, and our findings should be validated in other countries and among different ethnic groups in the future.

This study reveals a relatively high prevalence of osteosarcopenia in elderly T2DM patients, with significant associations identified between low FPG, male gender, and low ASMI as major risk factors. A higher ASMI was found to be protective against the development of osteosarcopenia, underscoring the importance of maintaining muscle mass in the management of T2DM. Our findings align with previous research, indicating that T2DM exacerbates both sarcopenia and osteoporosis, leading to a compounded risk of osteosarcopenia. This highlights the need for comprehensive screening and targeted interventions to address muscle and bone health concurrently in T2DM patients. However, the cross-sectional nature of the study limits the ability to establish causality, and future longitudinal studies are needed to confirm these associations and explore underlying mechanisms.

Statements & Declarations

This study was funded by the Health Commission of Chengdu and The First People's Hospital of Longquanyi District Chengdu. The authors declare no conflicts of interest related to this study. All authors have read and approved the final manuscript and agree with the order of authorship. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Author Contribution

T.X. and S.Z. contributed equally to this work and should be considered co-first authors.T.X.: Conceptualization, Methodology, Data Collection, Writing – Original Draft.S.Z.: Data Analysis, Interpretation of Results, Writing – Review & Editing.J.L.: Project Coordination, Supervision, Writing – Final Approval.T.L., M.L., and J.Y.: Data Collection, Investigation, Resources.

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No competing interests reported.

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published 19 Aug, 2024

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Prevalence and Risk Factors of Osteosarcopenia in Elderly Patients with Type 2 Diabetes

Status:

Journal Publication

Version 1

Abstract

Purpose

Methods

Results

Conclusions

BACKGROUND

SUBJECTS AND METHODS

Study Subjects

Methods

Statistical Analysis

RESULTS

Comparison of Clinical Characteristics Between T2DM-OS and T2DM-NOS

Single-Factor Analysis

Multifactorial Logistic Regression Analysis of Osteosarcopenia Occurrence in Elderly T2DM Patients

DISCUSSTIONS

High Prevalence of Osteosarcopenia in Elderly T2DM Patients

Male Gender as a Risk Factor for T2DM-OS

Low FPG as a Risk Factor for T2DM-OS

High ASMI as a Protective Factor Against T2DM-OS

Limitations

CONCLUSIONS

Statements & Declarations

Declarations

Author Contribution

References

Additional Declarations

Status:

Journal Publication

Version 1