Abstract
Objectives
This study aimed to clarify the association between intrinsic capacity (IC) and sarcopenia in hospitalized older patients.
Design
A cross-sectional study.
Setting
Hospital-based.
Participants
This study included 381 inpatients aged ≥ 60 years (225 men and 156 women).
Measurements
IC was evaluated in five domains defined by the World Health Organization: cognition (Mini-Mental State Examination), locomotion (Short Physical Performance Battery test), vitality (Short-Form Mini Nutritional Assessment), sensory (self-reported hearing and vision) and psychological (5-item Geriatric Depression Scale) capacities. IC composite score (0–5) was calculated based on five domains, with lower scores representing greater IC. Sarcopenia was defined in accordance with the criteria recommended by the Asian Working Group for Sarcopenia (AWGS) 2019. Multiple linear and logistic regressions were performed to explore the associations between IC composite score and IC domains with sarcopenia and its defining components.
Results
The mean age of 381 patients included was 81.95±8.42 years. Of them, 128 (33.6%) patients had sarcopenia. The median IC composite score was 1 (1, 2). Cognition, locomotion, vitality, sensory and psychological capacities were impaired in 22.6%, 63.5%, 18.9%, 27.3% and 11.3% of patients. Multiple linear regression analyses showed that favorable IC domain scores in cognition, locomotion and vitality were associated with a stronger handgrip strength. A higher vitality score was associated with a greater appendicular skeletal muscle mass index (ASMI), and a higher locomotion score was associated with a greater gait speed. The multiple logistic regression analysis showed that only vitality impairment was associated with sarcopenia. A higher IC composite score was associated with higher risks of sarcopenia, as well as low ASMI, handgrip strength and gait speed.
Conclusion
This study indicated that a more serious impairment of IC was associated with a greater risk of sarcopenia. Vitality was the domain most strongly associated with sarcopenia. IC may be employed to detect and manage sarcopenia.
Key words: Intrinsic capacity, sarcopenia, older adults
Introduction
Sarcopenia, a progressive and generalized skeletal muscle disorder, features ageing-associated decline in skeletal muscle mass and function (1), with a global prevalence of 10–27 % in adults aged 60 years and over (2). Sarcopenia related adverse outcomes, such as dysphagia, functional decline, falls, fractures, hospitalization and mortality (3, 4), have placed a considerable economic burden on the healthcare system. Compared to those without sarcopenia, the adults with sarcopenia have about a two-fold higher risk of hospitalization and have an annual increase of $2315.7 in medical expense per person (5). In addition, medical expenditure increases with the severity of sarcopenia (6). Therefore, sarcopenia should be screened and appropriately managed for all older adults.
Intrinsic capacity (IC) was first conceptualized by the World Health Organization (WHO) in the World report on ageing and health in 2015 (7). As recommended in the WHO guidelines for integrated care for older people (ICOPE), IC should be enhanced to reduce care dependency and promote healthy ageing (8, 9). IC is defined as “the composite of all the physical and mental capacities of an individual”, which covers five domains of cognition, locomotion, vitality, sensory, and psychological capacity. These five domains interact with each other closely, and are combined to reflect the whole health of an individual (10).
Each domain in IC has been reported to associate with sarcopenia or sarcopenia components (11, 12, 13, 14). According to the AWGS 2019, an older adult should be suspected of sarcopenia if any of the following clinical conditions presents, such as functional decline, depressive mood, cognitive impairment, or malnutrition (15). Older adults with impairments in locomotor capacity or vitality need to be assessed and managed for sarcopenia, according to the ICOPE guidelines (9). However, no studies have explored the associations of all IC domains with sarcopenia and focused on these domains together as IC composite concept to investigate the relationship between IC and sarcopenia. Therefore, the aim of this cross-sectional study was to investigate the association between IC domains and their composite with sarcopenia in older hospitalized Chinese adults. Our findings will enable clinical staff to better understand the role of IC in sarcopenia and explore the potential of ICOPE to manage sarcopenia.
Methods
Study design and participants
In this cross-sectional study, data were collected from the comprehensive geriatric assessment (CGA) database of the Geriatric Hospital of Nanjing Medical University in China. A total of 381 participants were recruited from June 2020 to February 2022, including 225 males and 156 females, with an average age of 81.95±8.42 years. Excluded were those with: (1) age<60 years; (2) Parkinson disease, mental illnesses and acute conditions (e.g., acute heart failure, acute cerebrovascular disease, acute coronary syndrome); (3) severe osteoarthritis in the knees or hips, or a new fracture; (4) incapability to provide informed consent due to aphasia, deafness, and blindness; (5) incomplete data about main variables. All participants received the CGA performed by two experienced and well-trained nurses, using a face-to-face questionnaire. Anthropometric and bioimpedance measurements were also recorded.
Sarcopenia assessment
As recommended by the Asian Working Group for Sarcopenia in 2019, a diagnosis of sarcopenia was established on both a low muscle mass (appendicular skeletal muscle mass index <7.0 kg/m2 for men and <5.7 kg/m2 for women) and a low muscle strength (handgrip strength <28 kg for men and <18 kg for women), and/or with a low physical performance (gait speed <1.0 m/s).
Skeletal muscle mass was measured by a bioelectrical impedance analysis (BIA) (Inbody S10, Korea), and ASMI (appendicular skeletal muscle mass/height2) was calculated. For an individual in a standing position, handgrip strength (HGS) was measured by a hand dynamometer (EH101; Camry, Zhongshan, China). After two times of measurement, the highest value of dominant hand strength was recorded. Gait speed (GS) (m/s) was calculated when an individual was instructed by a well-trained nurse to walk 6 meters at their natural speed.
IC assessment
Of the five IC domains, cognition was assessed using the Chinese version of Mini-Mental State Examination (MMSE) (16), a 30-point questionnaire. The education-specific cutoff points were used, with a score ≤17 indicating cognitive impairment in illiterate individuals, ≤20 in individuals with primary school education, and ≤24 in individuals with middle school or higher education. Locomotion was evaluated with the Short Physical Performance Battery test (SPPB) (17), with a score ≤9 indicating locomotion impairment. Vitality was assessed using the Short-Form Mini Nutritional Assessment (MNA-SF) (18), with a score ≤11 indicating vitality impairment. The self-reported hearing and vision status was used to evaluate the sensory capacity. Participants were asked if they had experienced any decline in vision and hearing. And a score of 0 was assigned to participants with intact vision and hearing, those with either vision or hearing impairment scored 1, and those with both vision and hearing impairments scored 2. The score≥1 was considered sensory impairment. Psychological capacity was assessed using the 5-item Geriatric Depression Scale (GDS-5) (19), with a score ≥2 indicating impairment. Each domain impairment was given a score of “1”, otherwise “0”. The IC composite score was calculated by adding the scores of the five domains, which ranged from 0 to 5, with a lower IC composite score indicating a greater intrinsic capacity.
Covariates
The sociodemographic and behavioral characteristics of participates were assessed via face-to-face interviews. Medical history (hypertension/diabetes/chronic obstructive pulmonary disease/coronary heart disease/osteoporosis/history of stroke/anemia) was obtained from medical records. The sociodemographic characteristics included age, sex, educational level (<9 years, 9–12 years or > 12 years), and marital status (married or widowed). Behavioral characteristics included current smoking habit (yes or no) and physical activity (≥3 times/week, <3 times/week or never). Physical activity was evaluated with the following question: “How many times a week do you take an exercise of more than 30 minutes?” Venous blood was sampled by trained nurses and then analyzed at the hospital's clinical laboratory.
Statistical analysis
All statistical analyses were performed with SPSS (Version 25.0). Continuous variables in a normal distribution were expressed as means ± standard deviations, otherwise median (interquartile range), while categorical variables were reported as percentages. The characteristics between the participants with and without sarcopenia were compared using the chi-squared test, Student t-test, and Mann-Whitney U test. To examine the relationship between IC domain scores (continuous variables) and sarcopenia components (ASMI, HGS and GS), multiple linear regression analysis was performed. Beta regression coefficient (β) with standard error (SE) were reported. In addition, two multiple logistic regression models were constructed to estimate the association between IC (including each impaired IC domains [dichotomic variables] and IC composite score) and sarcopenia, with sarcopenia or its defining components as dependent variables. The covariables adjusted in multiple linear regression analysis and multiple logistic regressions including age, history of stroke, osteoporosis and anemia, were identified based on the statistically significant variables in the univariable model. And odds ratios with 95% confidence intervals were reported. Statistically significant was defined with a p-value less than 0.05.
Results
Study participant characteristics
A total of 381 participants (mean age 81.95±8.42 years [range, 61–95years]; 225 [59.1%] men, 156 [40.9%] women) were included. Sarcopenia was defined in 128 participants (33.6%), who were further split into two groups (non-sarcopenia or sarcopenia). The sarcopenia group was significantly older than the non-sarcopenia group, and demonstrated higher prevalence of chronic diseases, such as osteoporosis, history of stroke and anemia. However, sociodemographic characteristics, such as sex, educational, marital status and lifestyle (like smoking and physical activity), showed no between-group differences. Furthermore, lower HGS, GS and ASMI were observed in the sarcopenia group (Table 1).
Table 1.
Characteristics of the older adults in the sarcopenia group and non-sarcopenia group
| Variables | Total (n=381) | Non-sarcopenia (n=253) | Sarcopenia (n=128) | χ2/Z/t | P-value |
|---|---|---|---|---|---|
| Age(years) | 81.95±8.42 | 80.68±8.87 | 84.46±6.81 | −4.611 | < 0.001 |
| Sex (%) | 1.025 | 0.311 | |||
| Men | 225(59.1) | 154(60.9) | 71(55.5) | ||
| Women | 156(40.9) | 99(39.1) | 57(44.5) | ||
| Education (%) | 1.662 | 0.197 | |||
| < 9 years | 101(26.5) | 63(24.9) | 38(29.7) | ||
| 9–12 years | 105(27.6) | 68(26.9) | 37(28.9) | ||
| > 12 years | 175(45.9) | 122(48.2) | 53(41.4) | ||
| marital status (%) | 2.283 | 0.131 | |||
| married | 327(85.8) | 222(87.7) | 105(82) | ||
| widowed | 54(14.2) | 31(12.3) | 23(18) | ||
| Physical activity (%) | 5.831 | 0.054 | |||
| ≥3 times/week | 205(53.8) | 145(57.3) | 60(46.9) | ||
| <3 times/week | 79(20.7) | 53(20.9) | 26(20.3) | ||
| never | 97(25.5) | 55(21.7) | 42(32.8) | ||
| Current smoking (%) | 35(9.2) | 25(9.9) | 10(7.8) | 0.436 | 0.509 |
| Diabetes (%) | 121(31.8) | 87(34.4) | 34(26.6) | 2.401 | 0.121 |
| Hypertension (%) | 228(59.8) | 15(59.3) | 78(60.9) | 0.096 | 0.756 |
| COPD (%) | 39(10.2) | 24(9.5) | 15(11.7) | 0.461 | 0.497 |
| Osteoporosis (%) | 74(19.4) | 35(13.8) | 39(30.5) | 15.029 | < 0.001 |
| Coronary heart disease (%) | 115(30.2) | 74(29.2) | 41(32.0) | 0.312 | 0.576 |
| History of stroke (%) | 176(46.2) | 106(42.2) | 70(54.7) | 5.288 | 0.021 |
| Anemia (%) | 151(39.6%) | 84(33.2%) | 67(52.3%) | 13.018 | < 0.001 |
| ALB (g/L) | 38.36±4.14 | 38.66±4.13 | 37.77±4.13 | 1.959 | 0.05 |
| CRP (mg/L) | 1.3(0.50,4.00) | 1.2(0.52,3.18) | 1.5(0.50,8.15) | −1.229 | 0.219 |
| HGS (kg) | 24.08±7.92 | 25.76±8.34 | 20.75±5.75 | 6.842 | < 0.001 |
| GS (m/s) | 0.7±0.25 | 0.73±0.26 | 0.62±0.23 | 4.401 | < 0.001 |
| ASMI (kg/m2) | 6.8(6,7.6) | 7.3(6.65,7.90) | 5.7(5.40,6.60) | −12.621 | < 0.001 |
Data were expressed as mean ± standard deviation, n (%) or M (P25, P75); Abbreviations: COPD, Chronic obstructive pulmonary disease; ALB, Albumin; CRP, C-reactive protein; HGS, handgrip strength; ASMI, Appendicular skeletal muscle mass index; GS, gait speed
The IC characteristics of participants are compiled in Table 2. Overall, the prevalence of IC impairment was 76.9%. Cognition impairment was found in 22.6%, locomotion impairment in 63.5%, vitality impairment in 18.9%, sensory impairment in 27.3% and psychological impairment in 11.3% of all participants. The sarcopenia group had lower scores in locomotion, vitality domains and higher scores in sensory, psychological domains than the non-sarcopenia group (all p <0.05). Additionally, the sarcopenia group had a higher prevalence of IC impairment (89.8% vs 70.4%) and higher percentages of impairment in cognition, locomotion, vitality and psychological domains than the non-sarcopenia group (all p <0.05). Furthermore, a higher IC composite score was observed in the sarcopenia group (p <0.001). A higher number of impaired domains was associated with a higher risk of sarcopenia (p <0.001) (Figure 1).
Table 2.
Comparison of IC between the sarcopenia group and the non-sarcopenia group
| Variables | Total (n=381) | Non-sarcopenia (n=253) | Sarcopenia (n=128) | χ2/z | P-value |
|---|---|---|---|---|---|
| Intrinsic capacity domains score | |||||
| Cognitive domain score | 27(25,28) | 27(25,28) | 27(24,28) | −1.901 | 0.057 |
| Locomotor domain score | 8(5,8) | 9(6,11) | 7(4,10) | −3.976 | < 0.001 |
| Vitality domain score | 13(12,14) | 14(13,14) | 12(10.25,13) | −8.619 | < 0.001 |
| Sensory domain score | 0(0,1) | 0(0,0) | 0(0,1) | −2.044 | 0.041 |
| Psychological domain score | 0(0,1) | 0(0,1) | 1(0,1) | −3.583 | < 0.001 |
| Impaired intrinsic capacity domains (%) | |||||
| Cognition | 86(22.6) | 47(18.6) | 39(30.5) | 6.877 | 0.009 |
| Locomotion | 242(63.5) | 147(58.1) | 95(74.2) | 9.527 | 0.002 |
| Vitality | 72(18.9) | 24(9.5) | 48(37.5) | 43.522 | < 0.001 |
| Sensory | 104(27.3) | 61(24.1) | 43(33.6) | 3.852 | 0.05 |
| Psychological | 43(11.3) | 22(8.7) | 21(16.4) | 5.047 | 0.025 |
| IC composite score | 1(1,2) | 1(0,2) | 2(1,3) | 5.741 | < 0.001 |
Data were expressed as n (%) or M (P25, P75); Abbreviations: IC, Intrinsic Capacity
Figure 1.
Percentages of sarcopenia and non-sarcopenia among hospitalized older patients according to the number of impaired IC domain
Abbreviations: IC, Intrinsic Capacity
Relationship between IC and sarcopenia
We further examined the association between IC domain scores and sarcopenia components (Table 3). In our multiple linear regression models, after adjusting for age, history of stroke, osteoporosis and anemia, a higher vitality score was associated with a greater ASMI (β=0.342, p<0.001). Higher scores in cognition (β=0.158, p=0.001), locomotion (β=0.295, p<0.001) and vitality domains (β=0.093, p=0.044) were associated with better handgrip strength. Locomotion domain score was also positively associated with gait speed (β=0.723, p<0.001). However, no significant association was observed between components of sarcopenia and sensory or psychological capacities.
Table 3.
Multiple linear regression evaluating association between IC domain scores and sarcopenia components
| ASMI | HGS | GS | |||||||
|---|---|---|---|---|---|---|---|---|---|
| β | SE | P-value | β | SE | P-value | β | SE | P-value | |
| Cognition | 0.082 | 0.015 | 0.099 | 0.158 | 0.099 | 0.001 | 0.011 | 0.002 | 0.325 |
| Locomotion | −0.014 | 0.023 | 0.829 | 0.295 | 0.146 | < 0.001 | 0.723 | 0.004 | < 0.001 |
| Vitality | 0.342 | 0.032 | < 0.001 | 0.093 | 0.204 | 0.044 | 0.007 | 0.005 | 0.205 |
| Sensory | −0.036 | 0.094 | 0.453 | 0.002 | 0.589 | 0.968 | 0.018 | 0.014 | 0.597 |
| Psychological | −0.011 | 0.064 | 0.830 | −0.019 | 0.406 | 0.677 | −0.037 | 0.010 | 0.284 |
Abbreviations: β, Beta regression coefficient; SE, Standard error; ASMI, Appendicular skeletal muscle mass index; HGS, Handgrip strength; GS, Gait speed. The model was adjusted for age, history of stroke, osteoporosis and anemia.
After adjusting for age, history of stroke, osteoporosis and anemia, the logistic regression analysis results showed that vitality impairment (OR: 4.521, 95%CI: 2.514–8.129) was significantly associated with a high risk of sarcopenia (Table 4). IC composite score (OR=1.563, 95%CI:1.247–1.958) was provided as an independent risk factor for sarcopenia. A higher IC composite score was also significantly associated with increased risks of low ASMI (OR=1.548, 95%CI:1.239–1.935), low HGS (OR=1.793, 95%CI:1.395–2.303) and low GS (OR=3.131, 95%CI:1.725–5.685) (Table 5).
Table 4.
Multiple logistic regression evaluating association between impaired IC domains and sarcopenia
| Impaired domains | B | SE | Wald | OR (95%CI) | P-value |
|---|---|---|---|---|---|
| Cognition | 0.219 | 0.294 | 0.557 | 1.245(0.7–2.214) | 0.455 |
| Locomotion | 0.026 | 0.324 | 0.006 | 1.026(0.544–1.937) | 0.936 |
| Vitality | 1.509 | 0.299 | 25.4 | 4.521(2.514–8.129) | < 0.001 |
| Sensory | 0.223 | 0.269 | 0.687 | 1.25(0.738–2.116) | 0.407 |
| Psychological | 0.354 | 0.375 | 0.889 | 1.424(0.683–2.972) | 0.346 |
Abbreviations: OR, Odds ratio; CI, Confidence interval; The model was adjusted for age, history of stroke, osteoporosis and anemia.
Table 5.
Multiple logistic regression evaluating association between IC composite score and sarcopenia with its components
| Sarcopenia | Low ASMI | Low HGS | Low GS | |||||
|---|---|---|---|---|---|---|---|---|
| OR (95% CI) | P-value | OR (95% CI) | P-value | OR (95% CI) | P-value | OR (95% CI) | P-value | |
| IC composite score | 1.563 (1.247–1.958) | < 0.001 | 1.548 (1.239–1.935) | < 0.001 | 1.793 (1.395–2.303) | < 0.001 | 3.131 (1.725–5.685) | < 0.001 |
Abbreviations: OR, Odds ratio; CI, Confidence interval; IC, Intrinsic Capacity; ASMI, Appendicular skeletal muscle mass index; HGS, Handgrip strength; GS, Gait speed; Low ASMI is <7.0 kg/m2 in men and <5.7 kg/m2 in women. Low HGS is <28 kg in men and <18 kg in women. Low GS is <1.0 m/s. The model was adjusted for age, history of stroke, osteoporosis and anemia.
Discussion
Our study is the first to investigate the relationship between IC and sarcopenia. We found that the prevalence of IC impairment was 89.9% in sarcopenia patients. Furthermore, cognition, locomotion and vitality domains were associated with components of sarcopenia. However, only vitality impairment was strongly associated with sarcopenia after adjustment for age, history of stroke, osteoporosis and anemia. In addition, the IC composite score was an independent risk factor for sarcopenia and deficits in its associated components. This finding highlights the clinical significance of IC in preventing, delaying or reversing sarcopenia among older hospitalized patients.
A cross-sectional study has reported that the prevalence of IC impairment is 39.9% in 5823 Chinese community-dwelling older adults (20). But, a higher prevalence (76.9%) was observed in this study, which is close to that in a hospital-based study (75.3%) (21) and slightly higher than that in an inpatient population (69.1%) (22). One potential explanation is that our patients are relatively older than the previous inpatient population, or that different tools have been used for assessing each domain of IC, despite the recommendations in WHO ICOPE guidelines (9).
The prevalence of sarcopenia varies with diagnostic criteria, muscle mass measurement methods, cut-off values, and populations. A systematic review has reported that the prevalence of sarcopenia ranges from 0.3% to 53% using AWGS criteria (2). Meanwhile, the prevalence of sarcopenia was 33.6% in this study, which is in line with those in another Chinese study using AWGS criteria (23) and Glisten study of older hospitalized patients using EWGSOP criteria (24). But our estimated prevalence was significant lower than that in the study enrolling patients from in-hospital rehabilitation wards (60%) (25) and higher than that estimated in community-dwelling populations (17.4%) (26).
According to the univariate analysis, sarcopenia was associated with impairments in cognition, locomotion, vitality, and psychological capacity. Our finding is consistent with a meta-analysis showing that malnutrition/malnutrition risk, cognitive impairment, and depression were associated factors of sarcopenia (27). We also found that sensory function impairment was more severe in the sarcopenia group. In line with our findings, a systematic review has suggested that adults with single or multiple sensory impairments, especially visual, hearing and smell impairments, are more likely to have sarcopenia (28).
Our multiple linear regression analysis revealed that cognition, locomotion and vitality domains were associated with components of sarcopenia. The association between locomotion and GS was expected. Locomotor capacity, which is defined as one's bodily capacity to move from one place to another, such as gait speed, reflects one's physical performance (9, 15). An interesting discovery was that HGS was positively associated with both vitality and locomotion, especially the latter. Consistent with Wu's report that the correlation of handgrip strength with SPPB is stronger than with vitality measurements (BMI, weight loss, and swallowing impairment), it may imply that handgrip strength should be used to measure locomotion (29). Although previous studies and the new consensus hold that handgrip strength is a candidate attribute of vitality capacity (30, 31, 32). So, it needs cohort studies to provide more stronger evidence. We found that a higher vitality score was associated with a greater ASMI. Moreover, in the multiple logistic regression analysis, only vitality impairment demonstrated to be associated with sarcopenia. However, theoretically, sarcopenia should be particularly correlated with impaired locomotor capacity, because low physical performance is one of the diagnostic criteria for sarcopenia (15). The strongest association between vitality and sarcopenia may be explained by that vitality was estimated through MNA-SF, a tool that measures nutritional status and collects anthropometric data (e.g., BMI) (33). In addition, reduced muscle mass, the predominant diagnostic reference for sarcopenia, can also be used to diagnose malnutrition, according to the Global Leadership Initiative on Malnutrition (GLIM) criteria (34). In the new consensus, body composition (i.e., BMI, muscle mass), malnutrition or nutritional status are two candidate attributes of vitality capacity (32). Vitality may moderate the relationship between cognition and sarcopenia. Liu et al. have conducted a cross-sectional study of 4023 community-dwelling older adults from West China, demonstrating that the direct effects of cognitive decline on sarcopenia disappears after nutritional status was absorbed into the mediation model analysis, which indicates that the relationship between cognitive decline and sarcopenia is mediated by nutritional status in older adults (35). Vitality is a physiological state that reflects in neuromuscular function, energy and metabolism, and immune and stress response functions of the body (32). Vitality is a core physiological determinant of IC, and interacts with other IC domains (30, 32, 36). Gaussens et al. first demonstrated that vitality impairment (appetite and weight loss) was associated with an increased likelihood of impairment in all the other IC domains (i.e., cognition, psychology, locomotion, vision, and hearing) (37). Vitality impairment may result in a hierarchical cascade of impairments in other IC domains (38). Therefore, malnutrition is targeted to manage sarcopenia (39). Older adults are especially susceptible to malnutrition, because of some ageing-associated physiological and pathological factors, such as anorexia of aging (40), poor oral health (41), micronutrient and mineral absorption deficiency, as well as low-rate metabolism (42). Protein intake is crucial for maintenance of muscle mass and strength. Additionally, vitamin D and micronutrients are essential for muscle health (43). Ageing is associated with reduced physical activity and appetite, leading to low energy requirements and inadequate food intake (44). An insufficient intake reduces the basal rate of muscle protein synthesis by approximately 20% (45). In contrast to a previous study which revealed that the GDS-15 score had negative associations with grip strength and walking speed (46), no association was observed between depression and any of diagnostic components of sarcopenia in the current study. We speculate that too few older adults have a depressive mood (11.3%) to make the relationship between depression and sarcopenia insignificant. A previous study showed an association between sensory impairments and sarcopenia (28), but we did not observe any association between sensory function and sarcopenia, after adjusting some confounding factors. The absence of association may be due to the sensory assessment self-reported, rather than instrumentally measured, in the current study.
Given that the five IC domains are closely interrelated (10), the IC composite score was calculated to reflect whole effect of IC in older adults. Although only impaired vitality was associated with sarcopenia among the five domains, IC composite score was independently associated with sarcopenia. A larger IC composite score or more IC impairments could indicate a higher risk of sarcopenia. Similarly, a large cross-sectional study in West China, with 2454 females aged 50 years or older, has revealed that those with only depression (OR=1.45, 95%CI=1.04–2.02), only visual impairment (OR=1.69, 95%CI=1.27–2.26), or both (OR=1.76, 95% CI=1.16–2.67) had a higher risk of sarcopenia than those without depression or visual impairment (47). We found that participants with more deficits in IC was significantly associated with increased risks of low ASMI, low HGS, and low GS. Ma et al also reported that participants with IC declines had worse walk speeds and grip strength (22). Conversely, Ramírez-Vélez et al revealed that older adults with an optimal handgrip strength had a better IC (48). The mechanism for the association between IC and sarcopenia has yet to be elucidated, but may lie in age-related chronic low-grade inflammation and mitochondrial dysfunction. Elevated circulating tumor necrosis factor receptor 1 (TNFR1), CRP or homocysteine level is related with IC decline (49, 50). Furthermore, numerous studies have demonstrated that some molecular pathways engaged in skeletal muscle wasting are activated by inflammatory cytokines, thus breaking the balance between protein synthesis and catabolism (51). Mitochondrial function is associated with IC domains through distinct mechanisms (52), which also causes metabolic abnormalities leading to quantitative and qualitative abnormalities in skeletal muscle (53).
The risk of sarcopenia increases with the loss of IC, implying that IC decline may be identified and multidomain interventions implemented to prevent or delay the development of sarcopenia. Nutritional and physical activity are essential for managing and preventing sarcopenia (39, 54). Our results may explain why the benefits of exercise are enhanced when combined with dietary supplementation (55). Some multidomain interventions can reverse sarcopenia among community-dwelling older adults. Lu et al. have reported that six months of multidomain lifestyle interventions (cognitive, nutritional, and physical interventions) were associated with reductions in sarcopenia (56). Another randomized control trial has shown that six months of integrated care (a combination of psychological, nutrition, and exercise interventions) improves sarcopenia status (57). The ICOPE is a person-centered and comprehensive care plan (9). Personalized interventions allow older people to be involved in their own care, so their adherence to interventions may be enhanced. Additionally, the pathway can overcome the fragmented management of sarcopenia. As ICOPE has just been recently proposed, there is a lack of relevant intervention studies. In this light, the present study suggests that ICOPE may be an effective approach to prevent and manage sarcopenia, especially its vitality domain.
The major strength of this study is that it is the first to examine the relationship between IC and sarcopenia. Moreover, the data from CGA database were collected by trained CGA nurses, which ensured the validity and consistency of data. Nevertheless, there are several limitations in our study. First, the causal association between IC and sarcopenia cannot be drawn because of the cross-sectional design of this study. Second, selection bias may exist, because our sample size was small and the average age of the participants was relatively older. More than half of older adults presented locomotor capacity impairment, and the effects of unhealthy conditions on physical performance could not be completely ruled out. These causes may be responsible for the unsignificant difference in impaired locomotor capacity between the sarcopenia group and the non-sarcopenia group. Therefore, further multi-center studies are needed. Third, some factors (e.g., tumour necrosis factor-α) related to sarcopenia were not measured. Finally, we evaluated skeletal muscle mass using BIA, the accuracy of which depends on various factors (e.g., temperature, humidity and skin condition), making it less reliable and consistent than Dual-emission X-ray absorptiometry (DXA) (58). But AWGS 2019 also recommended BIA for muscle-mass measurement to diagnose sarcopenia in clinical settings (15).
Conclusion
IC is independently associated with sarcopenia. In the five domains of IC, vitality has the strongest association with sarcopenia. IC, especially its vitality domain, may be employed to screen and manage sarcopenia in hospitalized older patients. Our study provides theoretical evidence for the potential of the ICOPE in intervening sarcopenia in older adults.
Acknowledgments
We acknowledge Yongzhen Mo and the Chronic Disease and Health Management Research Center for their guidance on statistical analyses.
Funding statement: This work was supported by a grant (BR2022070) from the Science and Technology Department of Jiangsu Province.
Ethical standards: This study was approved by the Ethics Committee of the Geriatric Hospital of Nanjing Medical University (Ethic number: 2020025). All participants provided informed consent prior to their participation in the study. This study was performed in accordance with the Declaration of Helsinki.
Conflicts of Interest: None declared.
References
- 1.Cruz-Jentoft A J, Sayer A A. Sarcopenia[J] Lancet. 2019;393(10191):2636–2646. doi: 10.1016/S0140-6736(19)31138-9. PubMed PMID: 31171417. [DOI] [PubMed] [Google Scholar]
- 2.Petermann-Rocha F, Balntzi V, Gray S R, et al. Global prevalence of sarcopenia and severe sarcopenia: a systematic review and meta-analysis[J] J Cachexia Sarcopenia Muscle. 2022;13(1):86–99. doi: 10.1002/jcsm.12783. PubMed PMID: 34816624. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Xia L, Zhao R, Wan Q, et al. Sarcopenia and adverse health-related outcomes: An umbrella review of meta-analyses of observational studies[J] Cancer Med. 2020;9(21):7964–7978. doi: 10.1002/cam4.3428. PubMed PMID: 32924316; PMCID 7643685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Beaudart C, Zaaria M, Pasleau F, et al. Health Outcomes of Sarcopenia: A Systematic Review and Meta-Analysis[J] PLoS One. 2017;12(1):e169548. doi: 10.1371/journal.pone.0169548. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Goates S, Du K, Arensberg M B, et al. Economic Impact of Hospitalizations in US Adults with Sarcopenia[J] J Frailty Aging. 2019;8(2):93–99. doi: 10.14283/jfa.2019.10. PubMed PMID: 30997923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Ye C, Zheng X, Aihemaitijiang S, et al. Sarcopenia and catastrophic health expenditure by socio-economic groups in China: an analysis of household-based panel data[J] J Cachexia Sarcopenia Muscle. 2022;13(3):1938–1947. doi: 10.1002/jcsm.12997. PubMed PMID: 35470981; PMCID 9178372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.WHO . World report on Ageing and Health. World Health Organization; Geneva: 2015. [Google Scholar]
- 8.WHO . Integrated Care for Older People: guidelines on Community-Level Interventions to Manage Declines in Intrinsic Capacity. World Health Organization; Geneva: 2017. [PubMed] [Google Scholar]
- 9.WHO . Integrated care for older people (ICOPE): guidance for person-centred assessment and pathways in primary care. World Health Organization; Geneva: 2019. [Google Scholar]
- 10.Cesari M, Araujo D C I, Amuthavalli T J, et al. Evidence for the Domains Supporting the Construct of Intrinsic Capacity[J] J Gerontol A Biol Sci Med Sci. 2018;73(12):1653–1660. doi: 10.1093/gerona/gly011. PubMed PMID: 29408961. [DOI] [PubMed] [Google Scholar]
- 11.Pang B, Wee S L, Lau L K, et al. Prevalence and Associated Factors of Sarcopenia in Singaporean Adults-The Yishun Study[J] J Am Med Dir Assoc. 2021;22(4):881–885. doi: 10.1016/j.jamda.2020.05.029. [DOI] [PubMed] [Google Scholar]
- 12.Kang S H, Jung D J, Cho K H, et al. Association between sarcopenia and hearing thresholds in postmenopausal women[J] Int J Med Sci. 2017;14(5):470–476. doi: 10.7150/ijms.18048. PubMed PMID: 28539823; PMCID 5441039. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Kim S H, Hurh K, Park Y, et al. Synergistic associations of visual and self-reported hearing acuity with low handgrip strength in older adults: a population-based cross-sectional study[J] BMC Geriatr. 2021;21(1):513. doi: 10.1186/s12877-021-02470-w. PubMed PMID: 34563124; PMCID 8466740. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Chang K V, Hsu T H, Wu W T, et al. Is sarcopenia associated with depression? A systematic review and meta-analysis of observational studies[J] Age Ageing. 2017;46(5):738–746. doi: 10.1093/ageing/afx094. PubMed PMID: 28633395. [DOI] [PubMed] [Google Scholar]
- 15.Chen L K, Woo J, Assantachai P, et al. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment[J] J Am Med Dir Assoc. 2020;21(3):300–307. doi: 10.1016/j.jamda.2019.12.012. PubMed PMID: 32033882. [DOI] [PubMed] [Google Scholar]
- 16.Zhang M Y, Katzman R, Salmon D, et al. The prevalence of dementia and Alzheimer's disease in Shanghai, China: impact of age, gender, and education[J] Ann Neurol. 1990;27(4):428–437. doi: 10.1002/ana.410270412. PubMed PMID: 2353798. [DOI] [PubMed] [Google Scholar]
- 17.Guralnik J M, Simonsick E M, Ferrucci L, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission[J] J Gerontol. 1994;49(2):M85–M94. doi: 10.1093/geronj/49.2.m85. PubMed PMID: 8126356. [DOI] [PubMed] [Google Scholar]
- 18.Rubenstein L Z, Harker J O, Salvà A, et al. Screening for undernutrition in geriatric practice: developing the short-form mini-nutritional assessment (MNA-SF)[J] J Gerontol A Biol Sci Med Sci. 2001;56(6):M366–M372. doi: 10.1093/gerona/56.6.m366. PubMed PMID: 11382797. [DOI] [PubMed] [Google Scholar]
- 19.Hoyl M T, Alessi C A, Harker J O, et al. Development and Testing of a Five-Item Version of the Geriatric Depression Scale[J] Journal of the American Geriatrics Society. 1999;47(7):873–878. doi: 10.1111/j.1532-5415.1999.tb03848.x. PubMed PMID: 10404935. [DOI] [PubMed] [Google Scholar]
- 20.Ma L, Chhetri J K, Zhang L, et al. Cross-sectional study examining the status of intrinsic capacity decline in community-dwelling older adults in China: prevalence, associated factors and implications for clinical care[J] BMJ Open. 2021;11(1):e43062. doi: 10.1136/bmjopen-2020-043062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Ma L, Zhang Y, Liu P, et al. Plasma N-Terminal Pro-B-Type Natriuretic Peptide Is Associated with Intrinsic Capacity Decline in an Older Population[J] J Nutr Health Aging. 2021;25(2):271–277. doi: 10.1007/s12603-020-1468-3. PubMed PMID: 33491044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Ma L, Chhetri J K, Zhang Y, et al. Integrated Care for Older People Screening Tool for Measuring Intrinsic Capacity: Preliminary Findings From ICOPE Pilot in China[J] Front Med (Lausanne) 2020;7:576079. doi: 10.3389/fmed.2020.576079. PubMed PMID: 33330532. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Hao Q, Hu X, Xie L, et al. Prevalence of sarcopenia and associated factors in hospitalised older patients: A cross-sectional study[J] Australas J Ageing. 2018;37(1):62–67. doi: 10.1111/ajag.12492. PubMed PMID: 29314585. [DOI] [PubMed] [Google Scholar]
- 24.Martone A M, Bianchi L, Abete P, et al. The incidence of sarcopenia among hospitalized older patients: results from the Glisten study[J] J Cachexia Sarcopenia Muscle. 2017;8(6):907–914. doi: 10.1002/jcsm.12224. PubMed PMID: 28913934; PMCID 5700449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Morandi A, Onder G, Fodri L, et al. The Association Between the Probability of Sarcopenia and Functional Outcomes in Older Patients Undergoing In-Hospital Rehabilitation[J] J Am Med Dir Assoc. 2015;16(11):951–956. doi: 10.1016/j.jamda.2015.05.010. PubMed PMID: 26089115. [DOI] [PubMed] [Google Scholar]
- 26.Ren X, Zhang X, He Q, et al. Prevalence of sarcopenia in Chinese community-dwelling elderly: a systematic review[J] BMC Public Health. 2022;22(1):1702. doi: 10.1186/s12889-022-13909-z. PubMed PMID: 36076194; PMCID 9454186. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Gao Q, Hu K, Yan C, et al. Associated Factors of Sarcopenia in Community-Dwelling Older Adults: A Systematic Review and Meta-Analysis[J]. Nutrients 2021;13(12): 10.3390/nu13124291 [DOI] [PMC free article] [PubMed]
- 28.Ho K C, Gupta P, Fenwick E K, et al. Association between age-related sensory impairment with sarcopenia and its related components in older adults: a systematic review[J] J Cachexia Sarcopenia Muscle. 2022;13(2):811–823. doi: 10.1002/jcsm.12930. PubMed PMID: 35229470; PMCID 8977955. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Wu W, Sun L, Li H, et al. Approaching person-centered clinical practice: A cluster analysis of older inpatients utilizing the measurements of intrinsic capacity[J] Front Public Health. 2022;10:1045421. doi: 10.3389/fpubh.2022.1045421. PubMed PMID: 36438281; PMCID 9692078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Beard J R, Jotheeswaran A T, Cesari M, et al. The structure and predictive value of intrinsic capacity in a longitudinal study of ageing[J] BMJ Open. 2019;9(11):e26119. doi: 10.1136/bmjopen-2018-026119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Beard J R, Si Y, Liu Z, et al. Intrinsic Capacity: Validation of a New WHO Concept for Healthy Aging in a Longitudinal Chinese Study[J] J Gerontol A Biol Sci Med Sci. 2022;77(1):94–100. doi: 10.1093/gerona/glab226. PubMed PMID: 34343305. [DOI] [PubMed] [Google Scholar]
- 32.Bautmans I, Knoop V, Amuthavalli T J, et al. WHO working definition of vitality capacity for healthy longevity monitoring[J] Lancet Healthy Longev. 2022;3(11):e789–e796. doi: 10.1016/S2666-7568(22)00200-8. PubMed PMID: 36356628; PMCID 9640935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Tan V, Pang B, Lau L K, et al. Malnutrition and Sarcopenia in Community-Dwelling Adults in Singapore: Yishun Health Study[J] J Nutr Health Aging. 2021;25(3):374–381. doi: 10.1007/s12603-020-1542-x. PubMed PMID: 33575731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Cederholm T, Jensen G L, Correia M, et al. GLIM criteria for the diagnosis of malnutrition - A consensus report from the global clinical nutrition community[J] Clin Nutr. 2019;38(1):1–9. doi: 10.1016/j.clnu.2018.08.002. PubMed PMID: 30181091. [DOI] [PubMed] [Google Scholar]
- 35.Liu X, Xia X, Hu F, et al. Nutrition status mediates the association between cognitive decline and sarcopenia[J] Aging (Albany NY) 2021;13(6):8599–8610. doi: 10.18632/aging.202672. PubMed PMID: 33714959. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Cesari M, Sadana R, Sumi Y, et al. What Is Intrinsic Capacity and Why Should Nutrition Be Included in the Vitality Domain?[J] J Gerontol A Biol Sci Med Sci. 2022;77(1):91–93. doi: 10.1093/gerona/glab318. PubMed PMID: 35015816. [DOI] [PubMed] [Google Scholar]
- 37.Gaussens L, González-Bautista E, Bonnefoy M, et al. Associations between Vitality/Nutrition and the Other Domains of Intrinsic Capacity Based on Data from the INSPIRE ICOPE-Care Program[J]. Nutrients 2023;15(7): 10.3390/nu15071567 [DOI] [PMC free article] [PubMed]
- 38.Yu R, Leung J, Leung G, et al. Towards Healthy Ageing: Using the Concept of Intrinsic Capacity in Frailty Prevention[J] J Nutr Health Aging. 2022;26(1):30–36. doi: 10.1007/s12603-021-1715-2. PubMed PMID: 35067700. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Cruz-Jentoft A J, Landi F, Schneider S M, et al. Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS)[J] Age Ageing. 2014;43(6):748–759. doi: 10.1093/ageing/afu115. PubMed PMID: 25241753; PMCID 4204661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Landi F, Calvani R, Tosato M, et al. Anorexia of Aging: Risk Factors, Consequences, and Potential Treatments[J] Nutrients. 2016;8(2):69. doi: 10.3390/nu8020069. PubMed PMID: 26828516; PMCID 4772033. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Azzolino D, Passarelli P C, De Angelis P, et al. Poor Oral Health as a Determinant of Malnutrition and Sarcopenia[J]. Nutrients 2019;11(12): 10.3390/nu11122898 [DOI] [PMC free article] [PubMed]
- 42.Inzitari M, Doets E, Bartali B, et al. Nutrition in the age-related disablement process[J] J Nutr Health Aging. 2011;15(8):599–604. doi: 10.1007/s12603-011-0053-1. PubMed PMID: 21968852. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Sieber C C. Malnutrition and sarcopenia[J] Aging Clin Exp Res. 2019;31(6):793–798. doi: 10.1007/s40520-019-01170-1. PubMed PMID: 31148100. [DOI] [PubMed] [Google Scholar]
- 44.Laviano A, Gori C, Rianda S. Sarcopenia and nutrition[J] Adv Food Nutr Res. 2014;71:101–136. doi: 10.1016/B978-0-12-800270-4.00003-1. PubMed PMID: 24484940. [DOI] [PubMed] [Google Scholar]
- 45.Pasiakos S M, Vislocky L M, Carbone J W, et al. Acute energy deprivation affects skeletal muscle protein synthesis and associated intracellular signaling proteins in physically active adults[J] J Nutr. 2010;140(4):745–751. doi: 10.3945/jn.109.118372. PubMed PMID: 20164371. [DOI] [PubMed] [Google Scholar]
- 46.Hayashi T, Umegaki H, Makino T, et al. Association between sarcopenia and depressive mood in urban-dwelling older adults: A cross-sectional study[J] Geriatr Gerontol Int. 2019;19(6):508–512. doi: 10.1111/ggi.13650. PubMed PMID: 30884107. [DOI] [PubMed] [Google Scholar]
- 47.Luo S, Chen X, Hou L, et al. Comorbid Depressive Symptoms, Visual Impairment, and Sarcopenia among Middle-Aged and Older Women: Findings from the West China Health and Aging Trend study[J] J Nutr Health Aging. 2021;25(9):1131–1137. doi: 10.1007/s12603-021-1687-2. PubMed PMID: 34725673. [DOI] [PubMed] [Google Scholar]
- 48.Ramírez-Vélez R, Correa-Bautista J E, García-Hermoso A, et al. Reference values for handgrip strength and their association with intrinsic capacity domains among older adults[J] J Cachexia Sarcopenia Muscle. 2019;10(2):278–286. doi: 10.1002/jcsm.12373. PubMed PMID: 30843369; PMCID 6463468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Ma L, Liu P, Zhang Y, et al. High Serum Tumor Necrosis Factor Receptor 1 Levels Are Related to Risk of Low Intrinsic Capacity in Elderly Adults[J] J Nutr Health Aging. 2021;25(4):416–418. doi: 10.1007/s12603-020-1533-y. PubMed PMID: 33786556. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Giudici K V, de Souto B P, Guerville F, et al. Associations of C-reactive protein and homocysteine concentrations with the impairment of intrinsic capacity domains over a 5-year follow-up among community-dwelling older adults at risk of cognitive decline (MAPT Study)[J] Exp Gerontol. 2019;127:110716. doi: 10.1016/j.exger.2019.110716. PubMed PMID: 31493520. [DOI] [PubMed] [Google Scholar]
- 51.Jo E, Lee S, Park B, et al. Potential mechanisms underlying the role of chronic inflammation in age-related muscle wasting[J] Aging clinical and experimental research. 2012;24(5):412–422. doi: 10.3275/8464. PubMed PMID: 22717404. [DOI] [PubMed] [Google Scholar]
- 52.Aragoni D S J, Rolland Y, Martinez L O, et al. Mitochondrial Dysfunction and Intrinsic Capacity: Insights From a Narrative Review[J] J Gerontol A Biol Sci Med Sci. 2023;78(5):735–742. doi: 10.1093/gerona/glac227. [DOI] [PubMed] [Google Scholar]
- 53.Nishikawa H, Fukunishi S, Asai A, et al. Pathophysiology and mechanisms of primary sarcopenia (Review)[J] International journal of molecular medicine. 2021;48(2):1. doi: 10.3892/ijmm.2021.4989. [DOI] [PubMed] [Google Scholar]
- 54.Dent E, Morley J E, Cruz-Jentoft A J, et al. International Clinical Practice Guidelines for Sarcopenia (ICFSR): Screening, Diagnosis and Management[J] J Nutr Health Aging. 2018;22(10):1148–1161. doi: 10.1007/s12603-018-1139-9. PubMed PMID: 30498820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Denison H J, Cooper C, Sayer A A, et al. Prevention and optimal management of sarcopenia: a review of combined exercise and nutrition interventions to improve muscle outcomes in older people[J] Clin Interv Aging. 2015;10:859–869. doi: 10.2147/CIA.S55842. PubMed PMID: 25999704; PMCID 4435046. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Lu Y, Niti M, Yap K B, et al. Assessment of Sarcopenia Among Community-Dwelling At-Risk Frail Adults Aged 65 Years and Older Who Received Multidomain Lifestyle Interventions: A Secondary Analysis of a Randomized Clinical Trial[J] JAMA Netw Open. 2019;2(10):e1913346. doi: 10.1001/jamanetworkopen.2019.13346. PubMed PMID: 31617926; PMCID 6806429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Chan D D, Tsou H H, Chang C B, et al. Integrated care for geriatric frailty and sarcopenia: a randomized control trial[J] J Cachexia Sarcopenia Muscle. 2017;8(1):78–88. doi: 10.1002/jcsm.12132. PubMed PMID: 27897406. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Chen L K, Liu L K, Woo J, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia[J] J Am Med Dir Assoc. 2014;15(2):95–101. doi: 10.1016/j.jamda.2013.11.025. PubMed PMID: 24461239. [DOI] [PubMed] [Google Scholar]