Abstract
This study aimed to identify the correlation of serum 25(OH)D level with sarcopenia and its components in Chinese elderly aged 65 years and above from rural areas. A total of 368 Chinese elderly aged 65 years and above in rural areas were enrolled. Indicators of muscle mass and strength, including the appendicular skeletal muscle mass (ASM), skeletal muscle index (SMI) and hand grip strength (HGS) were measured. Physical performance was assessed by the Short Physical Performance Battery (SPPB). Serum 25(OH)D levels were measured using the liquid chromatography with tandem mass spectrometry. Correlations of serum 25(OH)D level with sarcopenia and its components in Chinese elderly were identified by the binary logistic regression and linear regression analyses. The median serum 25(OH)D level was 34.80 ng/ml, and significantly higher in men than in women (40.70 ng/ml vs. 27.30 ng/ml). The prevalence of sarcopenia in our cohort was 21.5%, and higher in men than in women (29.4% vs. 10.8%). The serum 25(OH)D level was not correlated with sarcopenia, HGS and SPPB score in either male or female elderly. Positive correlations of age with sarcopenia, low HGS and low SPPB score were observed in male elderly, while significant correlations were not observed in females. Correlation analyses of sarcopenia components revealed that age was negatively correlated with SMI and gait speed in male elderly, but negatively correlated with the gait speed and positively correlated with the time to complete 5 sit-to-stand movements in female elderly. In conclusion, rural Chinese elderly have relatively high vitamin D level and prevalence of sarcopenia. Age but not serum 25(OH)D level is significantly correlated with sarcopenia in vitamin D sufficient male elderly.
Supplementary Information
The online version contains supplementary material available at 10.1038/s41598-025-85468-3.
Keywords: Vitamin D, Elderly, Sarcopenia, Hand grip strength, Physical performance, Age
Subject terms: Thyroid diseases, Geriatrics
Introduction
Sarcopenia is an aging-related disease characterized by progressive loss of skeletal muscle mass and decrease in muscle strength and/or physical fitness1. The prevalence of sarcopenia is on the rise across the world, and varies across regions mainly due to differences in demographic characteristics and diagnostic criteria. Epidemiologic investigations have reported the prevalence of sarcopenia in Asians older than 65 years ranging from 14.1 to 41.0%, which is much higher in older men2,3. Sarcopenia is a common risk factor of adverse events, such as falls, osteoporosis, fractures and metabolic syndrome in the elderly4. Many causes of sarcopenia have been proposed, including aging, malnutrition, low physical activity levels and vitamin D deficiency5.
Older adults are at a high risk of vitamin D deficiency due to low intestinal absorption, insufficient sun exposure and impaired cutaneous and kidney synthesis. An inflated prevalence of vitamin D deficiency at 35.7% is observed in Chinese elderly aged 65 years and above, and it can be varied with sex and residence6. Animal experiments have revealed that vitamin D receptor (VDR) is present in mouse myoblasts and strongly associated with muscle strength and fitness7. The discovery of vitamin D receptors in human skeletal muscle has also led to speculation that vitamin D levels have a direct effect on muscle metabolism.
Serum 25(OH)D is the optimal indicator of vitamin D status8. Controversial results are obtained in the epidemiological studies on serum 25(OH)D and sarcopenia or its components in the elderly. Some believe that serum 25(OH)D levels in community-dwelling older adults are correlated with decreases in muscle mass and physical fitness and the incidence of sarcopenia9–11. Contrariwise, evidences have supported that 25(OH)D levels are not correlated with muscle strength and physical performances in Asians12,13. In addition, a sex-based difference in the correlation between 25(OH)D levels and sarcopenia has been detected in Chinese and South Korean people14,15.
Previous studies have focused on the muscle mass and/or physical fitness in young patients with sarcopenia. The components of sarcopenia, especially in older adults, have not been widely analyzed. In the present cross-sectional study involving the Chinese elderly aged 65 years and above in rural areas, we analyzed the correlation of serum 25(OH)D levels with sarcopenia and its components.
Results
Participants from the cohort in the TOPS study
Among the 1,309 older adults aged 65 years and above from Suining County, Xuzhou City, Jiangsu Province in the TOPS study initially enrolled in the present study, there were 613 (46.8%) females. The mean age and serum 25(OH)D level in 1,309 older adults were 72.19 ± 5.75 years and 33.50 (26.60–41.60) ng/ml, respectively. The incidence of vitamin D insufficiency in them was 7.6% (99/1,309), and it was significantly higher in females than that of males. Compared with those with vitamin D sufficiency, older adults with vitamin D insufficiency presented significantly higher BMI, FBG and HOMA-IR, but lower TC, HDL-C and LDL-C (Supplementary Table 1).
We compared baseline characteristics of 368 participants enrolled in our study and 1,309 participants from Suining County, Xuzhou City, Jiangsu Province in the TOPS study. Comparable age, sex, weight, BMI, 25(OH)D, blood glucose and blood lipids between two cohorts were suggestive of the representativeness of study samples (Supplementary Table 2).
Baseline characteristics of participants
Among the 386 Chinese elderly aged 65 years and above in our study, there were no significant differences in age and BMI between males and females (both P > 0.05). Serum 25(OH)D levels were significantly higher in male older adults than in female older adults (40.70 [33.80–43.80] ng/mL vs. 27.30 [22.45–34.0] ng/mL, P < 0.001). The prevalence of vitamin D insufficiency in our cohort was 7.3% (27/368), and significantly lower in males than in females (0.9% vs. 14.6%, P < 0.001). Compared to those of female older adults, males presented significantly lower HbA1c, FINS, HOMA-IR, TC, TG and LDL-C (all P < 0.05, Table 1).
Table 1.
Sex-based baseline characteristics of participants (n = 368).
| Total (n = 368) |
Male (n = 211) |
Female (n = 157) |
P value | |
|---|---|---|---|---|
| Age (years) | 71.36 ± 4.78 | 71.61 ± 4.64 | 71.02 ± 4.97 | 0.121 |
| 65–75 (n, %) | 280 (76.1) | 159 (75.4) | 121 (77.1) | 0.703 |
| ≥ 75 (n, %) | 88 (23.9) | 52 (24.6) | 36 (22.9) | |
| Height (cm) | 158.23 ± 8.25 | 162.74 ± 6.27 | 152.15 ± 6.50 | < 0.001 |
| Weight (kg) | 60.70 ± 10.04 | 63.79 ± 9.76 | 56.54 ± 8.87 | < 0.001 |
| BMI (kg/m2) | 24.24 ± 3.33 | 24.10 ± 3.32 | 24.44 ± 3.35 | 0.44 |
| Underweight (n, %) | 17 (4.6) | 13 (6.2) | 4 (2.5) | 0.423 |
| Healthy (n, %) | 162 (44.0) | 92 (43.6) | 70 (44.6) | |
| Overweight (n, %) | 139 (37.8) | 79 (37.4) | 60 (38.2) | |
| Obesity (n, %) | 50 (13.6) | 27 (12.8) | 23 (14.6) | |
| Waist circumstance (cm) | 90.70 ± 9.65 | 90.73 ± 9.27 | 90.66 ± 10.17 | 0.538 |
| Hip circumstance (cm) | 99.74 ± 8.84 | 100.12 ± 9.56 | 99.23 ± 7.77 | 0.157 |
| 25(OH)D (ng/ml) | 34.80 (26.60–42.88) | 40.70 (33.80–43.80) | 27.30 (22.45–34.0) | < 0.001 |
| Vitamin D insufficiency (n, %) | 25 (6.8) | 2 (0.9) | 23 (14.6) | < 0.001 |
| TSH (mIU/L) | 2.37 (1.66–3.72) | 2.33 (1.65–3.78) | 2.43 (1.73–3.65) | 0.664 |
| FBG (mM) | 5.36 (5.02–5.87) | 5.33 (5.03–5.84) | 5.38 (5.02–5.90) | 0.581 |
| HbAlc (%) | 5.70 (5.53–6.10) | 5.70 (5.50–6.0) | 5.80 (5.60–6.20) | 0.048 |
| FINS (µU/ml) | 4.95 (3.04–7.36) | 3.87 (2.22–6.24) | 6.40 (4.22–8.84) | < 0.001 |
| HOMA-IR | 1.20 (0.71–1.88) | 0.94 (0.52–1.60) | 1.63 (1.06–2.36) | < 0.001 |
| TC (mM) | 4.66 (4.08–5.38) | 4.46 (3.92–5.19) | 4.88 (4.23–5.58) | < 0.001 |
| TG (mM) | 1.18 (0.88–1.66) | 1.03 (0.81–1.42) | 1.31 (1.04–2.02) | < 0.001 |
| HDL-C (mM) | 1.31 (1.08–1.52) | 1.29 (1.07–1.55) | 1.33 (1.10–1.50) | 0.813 |
| LDL-C (mM) | 2.85 (2.33–3.40) | 2.72 (2.26–3.29) | 3.04 (2.48–3.43) | 0.015 |
| Calf circumference (cm) | 34.17 ± 3.22 | 34.45 ± 3.24 | 33.78 ± 3.16 | 0.029 |
| HGS (kg) | 26.24 ± 6.85 | 28.90 ± 6.86 | 22.67 ± 4.96 | < 0.001 |
| Low HGS (n, %) | 123 (33.4) | 94 (44.5) | 29 (18.5) | < 0.001 |
| SMI (kg/m2) | 7.11 ± 1.0 | 7.41 ± 0.71 | 6.71 ± 1.18 | < 0.001 |
| 6-meter gait speed (m/s) | 1.03 ± 0.20 | 1.06 ± 0.19 | 0.98 ± 0.21 | 0.001 |
| Time to complete 5 sit-to-stand movements (s) | 16.01 ± 3.97 | 15.91 ± 4.39 | 16.15 ± 3.33 | 0.087 |
| SPPB ≤ 9 points (n, %) | 143 (38.9) | 61 (28.9) | 82 (52.2) | < 0.001 |
| Sarcopenia (n, %) | 79 (21.5) | 62 (29.4) | 17 (10.8) | < 0.001 |
BMI, body mass index; FBG, fasting blood glucose; FINS, fasting insulin; HbA1c, glycated hemoglobin; HOMA-IR, homeostasis model assessment of insulin resistance; HDL-C, high density lipoprotein cholesterol; LDL-C, low density lipoprotein cholesterol; TC, total cholesterol; TG, triglyceride; 25(OH)D, 25-hydroxyvitamin D; HGS, handgrip strength; SMI, skeletal muscle index; SPPB, Short Physical Performance Battery.
The prevalence of sarcopenia in our cohort was 21.5%, and significantly higher in males than in females (29.4% vs. 10.8%, P < 0.001). Physical performances in male older adults were significantly superior to females, including calf circumstance, HGS, adjusted SMI, 6-meter gait speed and SPPB score (all P < 0.05, Table 1).
Vitamin D-based subgroup differences in sarcopenia and its components
Participants were divided into three groups according to the tertiles of serum 25(OH)D levels. In male participants, the levels were divided into Q1 group (25(OH)D ≤ 35.80 ng/ml, n = 73), Q2 group (35.80 ng/ml < 25(OH)D ≤ 45.52 ng/ml, n = 68) and Q3 group (25(OH)D > 45.52 ng/ml, n = 70). Female participants were divided into Q1 group (25(OH)D ≤ 24.72 ng/ml, n = 52), Q2 group (24.72 ng/ml < 25(OH)D ≤ 30.94 ng/ml, n = 53) and Q3 group (25(OH)D > 30.94 ng/ml, n = 52). We did not detect significant differences in neither the proportions of older adults with sarcopenia, low HGS and low SPPB score, nor the HGS, adjusted SMI, 6-meter gait speed and time to complete 5 sit-to-stand movements in male and female participants (all P > 0.05, Table 2).
Table 2.
Sarcopenia and its components in male and female participants stratified by serum 25(OH)D levels.
| Males (n = 211) |
Females (n = 157) |
|||||||
|---|---|---|---|---|---|---|---|---|
| Q1 (n = 73) | Q2 (n = 68) | Q3 (n = 70) | P value | Q1 (n = 52) | Q2 (n = 53) | Q3 (n = 52) | P value | |
| Calf circumference (cm) | 34.35 ± 3.40 | 34.40 ± 3.13 | 34.61 ± 3.22 | 0.966 | 34.54 ± 2.83 | 33.11 ± 3.39 | 33.68 ± 3.13 | 0.048 |
| HGS (kg) | 29.20 ± 6.81 | 29.48 ± 7.27 | 28.03 ± 6.49 | 0.356 | 22.76 ± 4.70 | 21.80 ± 4.05 | 23.46 ± 5.92 | 0.404 |
| Low HGS (%) | 29 (39.7) | 28 (41.2) | 37 (52.9) | 0.228 | 7 (13.5) | 14 (26.4) | 8 (15.4) | 0.181 |
| SMI (kg/m2) | 7.36 ± 0.67 | 7.47 ± 0.74 | 7.41 ± 0.73 | 0.657 | 6.53 ± 1.28 | 6.78 ± 1.07 | 6.82 ± 1.19 | 0.467 |
| 6-meter gait speed (m/s) | 1.04 ± 0.21 | 1.06 ± 0.17 | 1.07 ± 0.19 | 0.617 | 0.96 ± 0.20 | 0.96 ± 0.22 | 1.03 ± 0.22 | 0.234 |
| Time to complete 5 sit-to-stand movements (s) | 15.95 ± 3.22 | 15.43 ± 3.91 | 16.33 ± 5.71 | 0.534 | 16.41 ± 3.89 | 16.06 ± 3.37 | 15.98 ± 2.67 | 0.986 |
| SPPB ≤ 9 points (n, %) | 22 (30.1) | 16 (23.5) | 23 (32.9) | 0.463 | 29 (55.8) | 24 (45.3) | 29 (55.8) | 0.461 |
| Sarcopenia (%) | 22 (30.1) | 18 (26.5) | 22 (31.4) | 0.803 | 8 (15.4) | 3 (5.7) | 6 (11.5) | 0.271 |
Male participants were divided into Q1 group (25(OH)D ≤ 35.80 ng/ml, n = 73), Q2 group (35.80 ng/ml < 25(OH)D ≤ 45.52 ng/ml, n = 68) and Q3 group (25(OH)D > 45.52 ng/ml, n = 70). Female participants were divided into Q1 group (25(OH)D ≤ 24.72 ng/ml, n = 52), Q2 group (24.72 ng/ml < 25(OH)D ≤ 30.94 ng/ml, n = 53) and Q3 group (25(OH)D > 30.94 ng/ml, n = 52).
Q, quartile; 25(OH)D, 25-hydroxyvitamin D; HGS, handgrip strength; SMI, skeletal muscle index; SPPB, Short Physical Performance Battery.
Correlation of serum 25(OH)D levels with sarcopenia and its components
A multiple linear regression analysis was performed to identify the correlations of covariates with components of sarcopenia, including HGS, adjusted SMI, 6-meter gait speed and time to complete 5 sit-to-stand movements (Table 3). In male older adults, age was negatively correlated with adjusted SMI (β = −0.210, P = 0.04) and 6-meter gait speed (β = −0.068, P = 0.026). In females, age was negatively correlated with 6-meter gait speed (β = −0.615, P < 0.001), but positively correlated with the time to complete 5 sit-to-stand movements (β = 2.366, P < 0.001). Age-based subgroup analysis further highlighted the above correlations in older adults aged 75 years and above than in those aged 65–75 years. However, we did not observe correlations of serum 25(OH)D levels with HGS, adjusted SMI, 6-meter gait speed and time to complete 5 sit-to-stand movements in neither male nor female participants.
Table 3.
A multivariate linear regression of sex-based correlations of serum 25(OH)D levels with sarcopenia and its components.
| HGS | SMI | 6-meter gait speed | Time to complete 5 sit-to-stand movements | |||||
|---|---|---|---|---|---|---|---|---|
| β (SE) | P value | β (SE) | P value | β (SE) | P value | β (SE) | P value | |
| Male | ||||||||
| Age ≥ 75 years | − 1.885 (1.089) | 0.085 | − 0.210 (0.105) | 0.04 | − 0.068 (0.031) | 0.026 | 0.683 (0.706) | 0.335 |
| BMI | 0.186 (0.142) | 0.192 | 0.083 (0.014) | < 0.001 | − 0.002 (0.004) | 0.548 | 0.006 (0.092) | 0.947 |
| Serum 25(OH)D | − 0.041 (0.042) | 0.334 | 0.004 (0.004) | 0.371 | 0.000 (0.001) | 0.728 | 0.006 (0.027) | 0.814 |
| Female | ||||||||
| Age ≥ 75 years | 0.436 (0.955) | 0.648 | 0.015 (0.214) | 0.944 | 0.165 (0.040) | < 0.001 | 2.366 (0.607) | < 0.001 |
| BMI | 0.203 (0.122) | 0.098 | 0.129 (0.027) | < 0.001 | − 0.003 (0.005) | 0.607 | 0.218 (0.078) | 0.006 |
| Serum 25(OH)D | 0.023 (0.046) | 0.612 | 0.013 (0.010) | 0.220 | 0.001 (0.002) | 0.698 | − 0.005 (0.029) | 0.859 |
The enter method was applied to this model, and adjusted analysis adjusted for age, BMI, waist circumstance, hip circumstance, calf circumference, TC, TG, HDL-C, LDL-C, HbA1c and HOMA-IR. All models included the same variables and categorizations/groupings, for visual presentation only significant variable categories are presented.
Β, regression coefficient; SE, standard error; 25(OH)D, 25-hydroxyvitamin D; HGS, handgrip strength; SMI, skeletal muscle index.
The prevalence of sarcopenia in 211 men and 157 women aged 65 years and above was 29.4% and 10.8%, respectively. Among them, 44.5% of men and 18.5% of women were assessed with low HGS, and 28.9% of men and 55.2% of women were graded with low SPPB scores. No significant differences in serum 25(OH)D levels were detected in male participants with sarcopenia (40.25 [33.28–49.70] ng/ml vs. 40.90 [34.30–47.95] ng/ml, P = 0.939), low HGS (41.40 [33.73–50.25] ng/ml vs. 38.90 [33.80–47.0] ng/ml, P = 0.150) and low SPPB scores (41.20 [33.75–48.85] ng/ml vs. 40.35 [33.80–48.15] ng/ml, P = 0.952) than in their counterparts. Similarly, we did not detect significant differences in serum 25(OH)D levels in female participants with sarcopenia (25.60 [20.65–36.10] ng/ml vs. 27.35 [22.53–32.90] ng/ml, P = 0.674), low HGS (26.90 [25.05–31.85] ng/ml vs. 27.30 [22.33–34.35] ng/ml, P = 0.516) and low SPPB scores (27.40 [22.40–34.23] ng/ml vs. 26.90[22.90–31.50] ng/ml, P = 0.917) than those of counterparts (data not shown).
A multivariate logistic regression analysis was conducted to further identify the independent effect of serum 25(OH)D levels on sarcopenia, low HGS and low SPPB scores (Table 4). Compared with those older adults aged 65–75 years, the odds ratios (ORs) of sarcopenia, low HGS and low SPPB scores in male participants older than 75 years were2.018 (95% CI 1.065–4.466), 2.018 (95% CI 1.086–3.974) and 3.269 (95% CI 1.673–6.388) with 1-year increase in age, respectively. However, age was not significantly correlated with sarcopenia, low HGS and low SPPB scores in female participants. Regardless of the sex, serum 25(OH)D levels were not correlated with sarcopenia, low HGS and low SPPB scores in older adults aged 65 years and above.
Table 4.
Logistic regression analyses of sex-based correlations of serum 25(OH)D levels with sarcopenia, low hand grip strength and low physical performances.
| Unadjusted sarcopenia | Adjusted sarcopenia | Unadjusted low HGS | Adjusted low HGS | Unadjusted low SPPB | Adjusted low SPPB | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| OR (95% CI) | P value | OR (95% CI) | P value | OR (95% CI) | P value | OR (95% CI) | P value | OR (95% CI) | P value | OR (95% CI) | P value | |
| Male | ||||||||||||
| Age ≥ 75 years | 1.95 (1.01–3.765) | 0.047 | 2.018 (1.065–4.466) | 0.033 | 2.024 (1.073–3.819) | 0.029 | 2.078 (1.086–3.974) | 0.027 | 3.164 (1.637–6.113) | 0.001 | 3.269 (1.673–6.388) | 0.001 |
| BMI | 0.773 (0.692–0.864) | < 0.001 | 0.769 (0.687–0.87) | < 0.001 | 0.968 (0.891–1.051) | 0.438 | 0.97 (0.892–1.056) | 0.485 | 1.01 (0.923–1.015) | 0.826 | 1.005 (0.917–1.012) | 0.916 |
| Serum 25(OH)D | 1.001 (0.975–1.028) | 0.916 | 0.995 (0.968–1.024) | 0.744 | 1.017 (0.992–1.042) | 0.18 | 1.013 (0.988–1.039) | 0.310 | 0.99 (0.964–1.018) | 0.486 | 0.988 (0.96–1.016) | 0.397 |
| Female | ||||||||||||
| Age ≥ 75 years | 2.679 (0.939–7.647) | 0.066 | 2.016 (0.65–6.225) | 0.225 | 2.518 (1.057–5.998) | 0.037 | 2.396 (0.981–5.855) | 0.055 | 2.172 (0.996–4.736) | 0.051 | 2.033 (0.924–4.477) | 0.078 |
| BMI | 0.682 (0.551–0.844) | < 0.001 | 0.687 (0.552–0.854) | 0.001 | 0.882 (0.772–1.007) | 0.063 | 0.904 (0.788–1.037) | 0.15 | 0.931 (0.846–1.024) | 0.141 | 0.937 (0.848–1.035) | 0.198 |
| Serum 25(OH)D | 0.999 (0.944–1.058) | 0.985 | 0.981 (0.92–1.046) | 0.553 | 1.025 (0.98–1.071) | 0.28 | 1.018 (0.972–1.065) | 0.449 | 0.995 (0.96–1.031) | 0.763 | 0.991 (0.955–1.029) | 0.632 |
The enter method was applied to this model and adjusted analysis adjusted for age, BMI, waist circumstance, hip circumstance, calf circumference, TC, TG, HDL-C, LDL-C, HbA1c and HOMA-IR. All models included the same variables and categorizations/groupings, for visual presentation only significant variable categories are presented.
OR, odds ratio; CI, confidence interval; 25(OH)D, 25-hydroxyvitamin D; HGS, handgrip strength; SPPB, short physical performance battery.
Discussion
In the present cross-sectional study involving 368 Chinese elderly aged 65 years and above in rural areas, the population had overall sufficient vitamin D levels. The prevalence of sarcopenia was 21.5%, and significantly higher in males than in females. Regardless of the sex, serum 25(OH)D levels were not correlated with sarcopenia and its components. Similarly, the prevalence of sarcopenia, muscle strength and mass and physical performances was comparable in male and female participants stratified by serum 25(OH)D levels. Age was independently correlated with sarcopenia in male older adults in positive manners, while no such association was found in females. This suggests that age, but not vitamin D levels, is independently associated with the prevalence of sarcopenia in older men living in vitamin D-sufficient rural areas of China.
The median vitamin D level of our study population was 34.80 ng/ml, and the proportion of vitamin D insufficiency was significantly lower than data from the China National Nutrition and Health Survey (CNNHS) and China Longitudinal Healthy and Longevity Survey (CLHLS)6,16. Although the production and metabolism of vitamin D decline with age, vitamin D levels in the elderly population are significantly lower than in the general adult population. However, vitamin D levels are diversely influenced by age, sex, region, season, sunshine time and lifestyle17. A 15-minute exposure to sunlight contributes to a massive cutaneous production of vitamin D even in the elderly18. Hence, sunlight exposure is the important source to get enough vitamin D in the elderly, even though its production decreases with age. Zhu et al.19 reported a summer serum vitamin D level of 29.7 ng/ml in elderly people in Shanghai, China, relatively similar to the population vitamin D level in our study. Given that our blood samples were also collected in summer, when sunlight is more abundant, this may have led to a higher overall vitamin D level in the population than in other seasonal samples. Outdoor activities can also affect vitamin D levels. A cohort study involving older adults in the Netherlands reported that serum 25(OH)D levels in winter are significantly lower than those in summer, and that elderly people spending more time outdoors have higher vitamin D levels20. Hibler et al.21 suggested that an hour of moderate-intensity physical activities per week increases 1,25(OH)2D levels by 0.80 pg/ml. Our population was selected from a rural area in northern China, where studies have shown that a high proportion of the older population engage in regular weekly physical activity22. In addition, most of the elderly in the area have access to enough sunlight and outdoor activities, as summer is the agricultural season in the area. We therefore speculate that these reasons may be the explanation for the higher serum 25(OH)D level in our population.
Previous studies have shown that vitamin D levels may play a potential role in maintaining or improving muscle strength, function and physical performance in older adults. There may also be an association with the development of sarcopenia. In a systematic review by Nascimento et al.23, the global prevalence of sarcopenia in older people ranged from 5% (95% [CI] 1–10%) in EWGSOP2 to 17% (95% [CI] 11–23%) in IWGS. Using the diagnostic criteria of sarcopenia in Asian and Chinese population, the prevalence of sarcopenia in the present study was similar to that previously reported24,25. In our study, no association was found between serum 25(OH)D levels and sarcopenia and its components in older men and women. A cross-sectional study in Japan found no significant association between vitamin D and physical performance, muscle strength, and fractures in older people, with a population mean vitamin D level of 31.94 ng/mL26. A recent study in postmenopausal women also found a lack of strong associations between 25(OH)D levels and muscle strength and physical performance in a population with a mean 25(OH)D level of 45.6 ng/dl27. Considering that the overall vitamin D levels in these studies were high, we hypothesised that this non-correlation may be caused by the low proportion of vitamin D deficiency in these subjects.
Obviously, the association between sarcopenia and its components and 25(OH)D concentrations may be more pronounced in populations where vitamin D deficiency is more prevalent. Data from a large study based on community-dwelling older adults showed that vitamin D deficiency was considered an important contributor to low grip strength and low physical performance in an older population with a prevalence of vitamin D insufficiency of more than half9. Conzade et al.10 found that low levels of vitamin D were significantly associated with increased odds of developing sarcopenia in an older population. Data from a multi-ethnic population study in western China also showed that vitamin D insufficiency was an independent predictor of sarcopenia in older men15. Vitamin D supplementation could significantly improve physical performance in older people with vitamin D deficiency11. These study results suggest that maintenance of relatively adequate levels of vitamin D in the elderly population may be more beneficial for physical performance and muscle strength.
The correlation of vitamin D with skeletal muscle and motor function has been validated in vivo experiments28. Girgis et al.7 detected the VDR deficiency is linked with sarcopenia and decreased grip strength and physical performances in mice. The presence of VDR is also observed in the nucleus of adult skeletal muscle. However, VDR is less expressed in human mature muscle fibers. The gradual decreases in the number of VDR in muscle tissues and responsiveness to vitamin D function during aging29,30. This may make the effects of vitamin D on skeletal muscle less significant in older people than in the general adult population31. Marantes et al.32 found that only in population under 65, lower vitamin D levels were significantly associated with reduced bone mass. In a cohort study of healthy participants, muscle strength and physical fitness are reduced with aging33,34. In our study, age appeared to weaken the association between vitamin D levels and in sarcopenia, declined muscle strength, and physical performance. We suggest that this may be due to the greater influence of age on physical performance and muscle strength during the ageing process in this population. After adjustment for confounders such as age and sex, vitamin D may not be a determinant.
The average BMI of our population was at the upper limits of the normal range, with a high proportion of overweight or obese older adults. This is similar to what we have seen in other studies of sarcopenia in older Asian populations3,35,36. The Irish Longitudinal Study on Ageing (ILS) found that overweight and obesity were associated with a lower likelihood of developing sarcopenia37, and the association between low BMI and sarcopenia appeared to predict the risk of malnutrition in the older population38. In our study, we also found a negative association between BMI and sarcopenia in the elderly population. We hypothesise that this negative correlation may be due to the fact that the nutritional status of overweight or obese people tends to be better, with more calories, protein and nutrients in their diets39. They may be healthier and at lower risk of sarcopenia than the underweight older population. In addition, LDL-c and TG levels were higher in older men than in women in our study, which may be related to factors such as dietary structure, lifestyle and vitamin D levels in the population. As a fat-soluble vitamin, vitamin D is involved in fat metabolism and may be a risk factor for metabolic syndrome6.
Furthermore, we observed a stronger correlation of age with sarcopenia and its components in male participants than in females, which may probably be attributed to the influence of sex hormones. A testosterone treatment increases type I and type II muscle fibers40. Decreases in sex hormones occur earlier in females than males. In older male adults, the influence of testosterone declines with aging on muscle mass is greater than that of changes in vitamin D levels41. This has led to gender differences in the development of sarcopenia and changes in muscle strength and fitness. However, no studies have been conducted to clarify the exact mechanism of these differences.
We made great efforts on minimizing the influences of race, lifestyle and cultural differences on sarcopenia and its components in Chinese elderly aged 65 years and above in rural areas through selecting a representative cohort and adopting a diagnostic criterion suitable for Asian people. However, there were several limitations of this study. First, it was a cross-sectional study in which we were unable to determine causal effects of serum 25(OH)D levels on sarcopenia and its components. Second, data of recent exogenous vitamin D supplementation, protein intake, physical activity levels and sunlight exposure were not available, leading to inability to assess and interpret vitamin D nutritional status of the population more specifically. Third, we didn’t collect data on the liver and kidney function of the population. Although we excluded older adults with severe or chronic liver and kidney disease by questionnaire and included as many covariates as possible in our analytical model, the final results may still be affected by confounding factors. Fourth, the study population was selected in rural China with generally adequate vitamin D levels, and the overall sample size was not large enough for further subgroup analyses, which limits our conclusions. In the future, we will further investigate the association between vitamin D levels and sarcopenia in the elderly population with a larger population and more diverse vitamin D nutritional status.
Taken together, we detected high serum 25(OH)D levels in summer, low prevalence of vitamin D insufficiency but high prevalence of sarcopenia especially in males in a cohort involving 368 Chinese elderly aged 65 years or above in rural areas. Regardless of gender, there was no significant association between serum 25(OH)D levels and sarcopenia and its components in the elderly population. Age seems to have a greater influence on muscle mass, strength and physical performance in vitamin D sufficient elderly.
Materials and methods
Participants
It was a cross-sectional study involving participants from the cohort of the Thyroid diseases in Older Population: Screening, Surveillance and Intervention (TOPS) study. The TOPS study was designed to determine reference ranges for thyroid-stimulating hormone (TSH) in specific age groups and observe the natural medical history of subclinical hypothyroidism (SCH) in 2,460 Chinese elderly aged 65 years and above in rural areas of Jiangsu Province through cluster sampling42–44. It was approved by the Ethics Committee of Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine. All methods were performed in accordance with the relevant guidelines and regulations. All participants in the TOPS study signed written informed consent, and those with severe parenchymatous diseases, mental illnesses and cognitive and communication disorders were excluded. Baseline assessment in the TOPS study was performed from May 2021 to June 2021, and all procedures were conducted strictly following relevant guidelines and regulations.
After excluding participants without complete clinical data of physical performance measurements and serum 25(OH)D levels, 1,309 older adults aged 65 years and above from Suining County, Xuzhou City, Jiangsu Province in the TOPS study were initially enrolled in the present study. An adequate sample size of 236 was established based on the estimates of the target population (n = 1,309), expected prevalence (25%), statistic corresponding to confidence level (95% CI) and allowable absolute deviation (5%)1,45. Subsequently, 600 participants were selected via stratified random sampling based on their age, sex and body mass index (BMI). Among them, 439 (73.1%) were willing to complete the measurements of sarcopenia components.
Then, participants with heart, lung, liver and kidney dysfunctions; infections, malignancies or other consumptive diseases; use of glucocorticoids, sex hormones, thyroid hormones and other drugs that may affect muscle function or bone metabolism; language, cognitive and hearing impairments or mental illnesses; or unable to cooperate with the testing were excluded. Finally, 368 eligible participants were enrolled in our study (Fig. 1).
Fig. 1.
Flow chart of participant enrollment.
Data collection and measurements of biochemical and metabolic indicators
Clinical data, including age, sex, height, weight, BMI, waist circumference, hip circumference, heart rate, blood pressure, blood lipids, fasting blood glucose (FBG), fasting insulin (FINS), medical history, medication history and history of falls, were recorded.
After an overnight fast of at least 8 h, 10 ml of venous blood of each participant was collected between 8 a.m. and 10 a.m. The supernatant serum sample obtained by a 15-min centrifugation at 1500×g was stored at −80 °C and sent for testing in the Laboratory of the Affiliated Hospital of Integrated Traditional Chinese and Western Medicine. Serum 25(OH)D was measured by the liquid chromatography with tandem mass spectrometry (LC-MS/MS). Total cholesterol (TC), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C) and FBG were measured by the ROCHE COBAS C702 biochemical analyzer via colorimetric method. Glycated hemoglobin (HbA1c) was measured using the D-10 high-performance liquid chromatography (HPLC) system.
Measurement of body composition and skeletal muscle mass
Appendicular skeletal muscle mass (ASM), defined as the sum of the skeletal muscle mass of the upper and lower extremities, and visceral fat area (VFA) were measured using a bioelectrical impedance analyzer (Inbody S10, Korea) by the same experienced investigator. Skeletal muscle index (SMI, kg/m2) was calculated by dividing ASM (kg) by the square of the height (m2).
Assessment of hand grip strength and physical performances
Hand grip strength was assessed using a digital dynamometer (Jamar® Smart Hand Dynamometer, Los Angeles, CA, USA) which measures between 0 and 90 kg of force with minimum measurement unit is 0.1 kg. The participant was asked to sit on a chair, abduct the elbow within 30° and bend the elbow at 90° between the upper arm and forearm. Participants were instructed to use their dominant hand to squeeze the dynamometer with maximum strength three times at 1-minute intervals. The maximum value of the three trials was recorded as hand grip strength (HGS).
Physical performances were assessed using the Short Physical Performance Battery (SPPB). The SPPB scores of the gait speed test, chair stand test and balance test were graded to assess physical performances, with 4 points of each test and 12 points in total. Decreases in the SPPB scores are closely related to the risk of frailty and disability among community-dwelling elderly people. The SPPB score of 0–6 points, 7–9 points and > 10 points suggested poor physical performances, high risk of all-cause mortality and good physical performances, respectively9. A score lower than 9 points in the SPPB test was suggestive of low physical performances. In the gait speed test, the participant was asked to walk straight from the start point to the 12-meter position at a normal pace for three times. The 6-meter gait speed was calculated by dividing the distance of 6 m by the time of walking straight from the 3-meter position to 9-meter position in the fastest way.
In the chair stand test, the participant was asked to stably and quickly stand up and sit down from a chair at the height of 46 cm for 5 times. The balance ability was assessed by standing unsupported for 10 s in each of three positions of together side-by-side, semi-tandem and tandem. A longer standing indicated a better physical performance.
Diagnostic criteria
Serum 25(OH)D measurements reflected the vitamin D status as follows: vitamin D deficiency, serum 25(OH)D level < 12 ng/ml (30 nmol/L); vitamin D insufficiency, 12 ng/ml ≤ serum 25(OH)D level < 20 ng/ml (50 nmol/L)8. In the present study, participants with less than 20 ng/mL serum 25(OH)D levels were diagnosed as vitamin D insufficiency; otherwise, they were confirmed as vitamin D sufficiency.
A sarcopenia diagnosis was made according to the criteria described in the Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment1. Low muscle mass was confirmed by an SMI < 7 kg/m2 in men and < 5.7 kg/m2 in women. Low muscle strength was confirmed by a grip strength < 28 kg in men and < 18 kg in women according to the Chinese expert consensus on diagnosis and treatment for elderly with sarcopenia 202125. Low physical performance was confirmed by either 6-meter gait speed < 1 m/s, or the time to complete 5 sit-to-stand movements ≥ 12 s or SPPB score ≤ 9 points9. Participants with low skeletal muscle mass combined with low muscle strength and/or low physical performance were diagnosed as sarcopenia.
Clinical data of BMI and HOMA-IR (Homeostatic Model Assessment for Insulin Resistance) were calculated using the simple formulas: BMI (kg/m2) = weight (kg) / height2 (m2); HOMA-IR = FBG (mmol/L) × FINS (µU/ml) / 22.5. A BMI of less than 18.5 kg/m2, 18.5 kg/m2 to 23.9 kg/m2, 24.0 kg/m2 to 27.9 kg/m2 and higher than 28.0 kg/m2 fell within the underweight, healthy weight, overweight and obesity ranges, respectively.
Statistical analysis
Statistical processing was performed using SPSS 26.0 (IBM Corporation, Armonk, NY, USA). The Kolmogorov-Smirnov test was applied to examine the normality. Normally distributed measurement data were expressed as mean ± standard deviation (
± SD), and differences were analyzed by the Student’s t-test or ANOVA; otherwise, they were expressed as the median (interquartile range [IQR]), and differences were analyzed by the Mann-Whitney U test or Kruskal-Wallis.
Sex-based subgroup differences in serum 25(OH)D levels and sarcopenia and its components were conducted. A multiple linear regression model involving dependent variables of HGS, multiple linear regression model, time to complete 5 sit-to-stand movements and adjusted SMI and the independent variable of serum 25(OH)D was created. Variables that reached statistical significance in the preliminary analyses were considered for inclusion in the model, and collinearity in the linear relationship was tested using scatter plots and variance inflation factor tests, with VIF ≤ 10 used as a diagnostic criterion for non-collinearity. Clinical applicability and potential factors from previous studies were also used to select covariates to enter the adjusted model. The stepwise(ENTER method) regression was performed in the multiple regression analysis. Multivariate logistic regression adjustment was later performed to calculate odds ratio (ORs) and corresponding 95% CI. A two-tailed p-value of less than 0.05 indicated a significant difference.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Author contributions
M.W., F.K., L.C. and X.S. were responsible for the overall design; S.Y. and Z.H. performed assessments of sarcopenia and its components; M.W., Z.H., Z.L., S.T., S.Y., X.S. were responsible for field investigation; Z.H., W.Z., L.X. and Z.L. were responsible for data collection; M.W. were responsible for statistical analysis and manuscript drafting; F.K. and X.S. revised the manuscript.
Funding
Medical Scientific Research Foundation of Jiangsu Province of China (Surface project) (M2020102); Jiangsu Provincial Key Research and Development Program (BE2020726); Suqian Key Research and Development Program (S202017, S202110); Geriatric Health Scientific Research Project of Jiangsu Province (LK2021059).
Data availability
The datasets generated and analyzed in the present study are available from the corresponding author upon reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Weinuo Mi and Huifeng Zhang have contributed equally to this work and shared the first authorship.
Contributor Information
Kuanlu Fan, Email: 15852161062@163.com.
Shuhang Xu, Email: shuhangxu@163.com.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets generated and analyzed in the present study are available from the corresponding author upon reasonable request.