Performance on sit-to-stand tests in relation to measures of functional fitness and sarcopenia diagnosis in community-dwelling older adults

Background The sit-to-stand (STS) test has been deployed as surrogate measures of strength or physical performance in sarcopenia diagnosis. This study examines the relationship of two common STS variants – Five Times Sit-to-Stand Test (5TSTS) and 30 s Chair Stand Test (30CST) – with grip strength, muscle mass and functional measures, and their impact on sarcopenia prevalence in community-dwelling older adults. Methods This is a cross-sectional analysis of 887 community-dwelling adults aged ≥50 years. Participants completed a battery of physical fitness tests - 5TSTS, 30CST, grip strength, gait speed, Timed-Up-and-Go (TUG) for dynamic balance and six-minute walk test (6MWT) for cardiorespiratory endurance. Muscle mass was measured using multi-frequency segmental bioelectrical impedance analysis (BIA). We performed correlation analysis between STS performance and other fitness measures and muscle mass, followed by multiple linear regression for the independent determinants of STS performance. Results Mean participant age was 67.3±7 years, with female predominance (72.9%). STS tests exhibited weak correlations with grip strength (30CST, r = 0.290; 5TSTS, r = − 0.242; both p< 0.01), and stronger correlations with gait speed (30CST, r = 0.517; 5TSTS, r = − 0.533; both p< 0.01), endurance (30CST, r = 0.558; 5TSTS, r = − 0.531; both p < 0.01) and dynamic balance (30CST, r = − 0.501; 5TSTS, r = 0.646; both p< 0.01). Muscle mass correlated with grip strength but not STS. In multiple regression analysis, all fitness measures were independently associated with 30CST performance. Performance in both STS tests remained independent of muscle mass. There was no significant difference in prevalence of possible sarcopenia diagnosis using grip strength or STS (30CST, 25.0%; 5TSTS, 22.1%; grip strength, 22.3%; p = 0.276). When both measures are used, prevalence is significantly higher (42.0%; p = 0.276). Prevalence of confirmed sarcopenia with inclusion of muscle mass was significantly lower using STS compared with grip strength (30CST, 4.6%; 5TSTS, 4.1% vs. grip strength, 7.1%; p< 0.05). Conclusion In the sarcopenia construct, STS tests better represents muscle physical performance rather than muscle strength. Different subsets of population with possible sarcopenia are identified depending on the test used. The lack of association of STS performance with muscle mass results in a lower prevalence of confirmed sarcopenia compared with grip strength, but may better reflect changes in muscle quality.


Introduction
Maintenance of functional fitness is necessary for avoiding mobility disability in an aging population. Muscle strength features as a key component of functional fitness, alongside aerobic endurance, flexibility and dynamic balance. Sarcopenia is characterized by age-related loss of skeletal muscle, and contributes to adverse health outcomes in older adults [1]. Muscle strength is regarded as the most reliable measure of muscle function and is the primary parameter of sarcopenia in the updated definition proposed by the European Working Group on Sarcopenia in Older People (EWGSOP2) [2]. While hand grip dynamometry has traditionally been used as a measure of muscle strength in the assessment of sarcopenia, lower body strength may better associate with functional activities and mobility tasks compared with grip strength, being necessary for Activities of Daily Living (ADLs) such as transfers, walking and stairs climbing [3]. From a broader perspective in Sarcopenia, optimal muscle quality as a primary physiological construct determines good muscle function. Muscle quality outcomes extend beyond strength and force production and includes intact metabolism, thermoregulation, signaling and myokine production [4]. Ideally, muscle assessments should also incorporate changes in muscle quality in aging.
Sit-to-Stand (STS) tests are used to evaluate lower body strength in the community [3,5,6], and are simple to set up, easily conducted by trained, non-medical people, and manageable in restricted spaces [7][8][9][10]. Test standardization protocols have been described [11], with normative values available both in Western and Asian populations [3,5,6,12]. Two commonly used STS test protocols are the time taken to complete five repetitions (5TSTS) [13] and the maximum number of chair stands within 30 s (30CST) [5]. The 30CST allows assessment of a wide range in ability and facilitates longitudinal monitoring of rehabilitation, as the 5TSTS may be limited by a floor effect in individuals with moderate to severe mobility limitations preventing completion of five repetitions [5]. Both tests are well validated with good test-retest and inter-rater reliability, and cutoff values for predicting adverse outcomes are available [14,15]. In addition, worse performance on STS tests are correlated with poorer muscle quality outcomes including ectopic fat infiltration in muscle (myosteatosis) from impaired muscle metabolism [4,16].
However, there is conflicting literature behind the fundamental construct underlying the STS test. It is unclear if STS tests better reflect muscle strength or physical performance in the diagnosis of sarcopenia. While STS is accepted as a proxy for lower limb strength in the revised EWGSOP2 operational diagnosis of sarcopenia [2], it is considered a surrogate measure for physical performance alongside gait speed and the Short Physical Performance Battery (SPPB) in the recent Asian Working Group for Sarcopenia (AWGS 2019) guidelines [9,17]. Nonetheless, both approaches are prevalent in literature. STS tests are still widely used as measures of strength [3,6], and are well correlated with objective strength testing such as leg-press resistance [5] and power-rigs [18]. However, prior studies suggest that STS is not a mere proxy for muscle strength, but also reflects endurance, balance and mobility [19]. While the 5TSTS test has been demonstrated to be an appropriate surrogate for gait speed in sarcopenia diagnosis [9], no study has yet examined the utility of 30CST as a measure of strength or physical performance despite it being an easier to perform STS test-variant in the elderly.
We hypothesize that in the sarcopenia construct, the 5TSTS and 30CST have stronger correlations to physical performance measures compared to muscle strength measures. We further hypothesize that the prevalence of sarcopenia will be significantly different if the STS tests were used instead of grip strength tests in conjunction with muscle mass measurements on BIA. Finally, we also aim to determine predictors of STS performance with a comprehensive set of demographic, health, social, behavioral and physical assessment variables.

Study population
The Individual Physical Proficiency Test for Seniors (IPPT-S) is an ongoing community-based programme designed to promote fitness and prevent or delay sarcopenia and frailty among older adults [20]. Eight hundred eighty-seven participants have since been recruited and included in this cross-sectional analysis. Ethics approval was obtained from Singhealth Institutional Review Board.
Eligible participants were aged > 50 years old, community dwelling and able to ambulate independently (with or without walking aids). Screening platforms were based at void decks of public housing blocks, senior activity centres and community clubs in the northeastern region of Singapore served by a regional healthcare facility. All participants completed a questionnaire-based multi-domain geriatric screen as well as physical fitness assessment administered by trained study team members. There were no exclusion criteria for participants as long as they were able to present themselves at the respective test centers and were well enough to undergo the fitness assessments.

Sit-to-stand test
Both the 30CST and 5TSTS were used in this study, in accordance with established protocols [5,21]. Participants were instructed to rise as quickly as possible from a seated position, with full body weight on the chair, to a standing posture, with their legs fully extended, while keeping their arms folded across their chest. The test administrator first demonstrated the execution of the test, and participants did not perform any physical test involving the lower limbs immediately prior to STS, to ensure performance would not be affected by fatigue. The 5TSTS measures the time taken, in seconds, to complete five repeated chair stands. The 30CST measures the maximal number of chair stands completed during 30 s of the test. Impaired performance on 5TSTS was defined using AWGS 2019 cut off > 12 s. Owing to the lack of establish cutoff on 30CST for sarcopenia diagnosis, we adopted the lowest quintile as indicative of impairment, in line with the approach of AWGS 2019 for weak handgrip strength [17].

Grip strength
Grip strength was measured using a JAMAR Plus Hand Dynamometer (Sammons Preston, Bolingbrook, IL, USA), following the Southampton protocol [22] with 2 trials for each hand, and alternating sides during the test. The maximal reading from all trials was used for analysis. Weak grip strength was defined using AWGS 2019 cutoffs < 28 kg for men and < 18 kg for women [17].

Timed-up-and-go
Dynamic balance was assessed using the Timed-Up-and-Go (TUG), in which participants had to rise from a chair, walk a distance of 3 m before turning and returning to a seated position [23]. Time taken, in seconds, was measured.

Habitual gait speed
Habitual gait speed was measured based on time taken to walk 10 m at usual pace, with a 2-m acceleration and deceleration zone before and after the timed section of 10 m [24]. Slow gait speed was defined using AWGS 2019 reference value of < 1.0 m/s [17].

Six minute walk test
Cardiorespiratory endurance was evaluated using the six-minute walk test (6MWT), in which participants had to walk as fast as they could along a 20-m path with encouragement throughout the test [25]. The total distance traversed in 6 min was recorded. Participants were allowed to rest at any time during the test if they reported significant fatigue or breathlessness.

Short physical performance battery
Participants completed tests of side-by-side, semi-tandem and tandem balance, and were scored on the SPPB by applying established cut-offs based on tests of usual gait speed and time to complete five chair stands [13]. A score < 9 was indicative of poor physical performance.

Skeletal muscle mass measurement
Appendicular skeletal muscle mass (ASM) was measured using multi-frequency segmental BIA (MC-780 M, TANI TA, Tokyo, Japan). Appendicular skeletal mass index (SMI) was calculated by summation of fat-free lean mass from all 4 limbs, normalized by the square of height (ASM/height 2 ). Participants with any metal implant were excluded from BIA. Measurements were taken before the commencement of physical tests and were taken, as per manufacturer's manual, in a standing upright position with feet and hands in contact with base electrodes and grip electrodes respectively. No specific instructions pertaining to hydration were given to participants prior to the test however all participants were screened via a short questionnaire to ensure they were feeling well and their blood pressure were normal before the tests. We defined low muscle mass using AWGS 2019 cutoff values of < 7.0 kg/m 2 and < 5.7 kg/m 2 for males and females respectively [17,26].

Fat mass index
We included Fat Mass Index (FMI) measurements as a proxy measure of muscle quality. Good correlations between increases in overall body fat and myosteatosis have been reported [27]. Appendicular fat mass (AFM) was measured using multi-frequency segmental BIA (MC-780 M, TANITA, Tokyo, Japan) following BIAvalidated methods described previously [28]. Appendicular fat mass index (FMI) was calculated by the summation of fat mass from all 4 limbs, normalized by the square of height (AFM/height 2 ) [29]. FMI incorporates height and body composition therefore it is a better measure than body mass index in reflecting nutritional status and physical performance [28][29][30].

Physical activity questionnaire
The type and amount of physical activity per week was recorded for all participants in a custom-designed questionnaire based on the Physical Activity Vital Sign Tool which in turn incorporates recommendations on physical activity from the American College of Sports Medicine (ACSM) and the American Heart Association (AHA) [31]. Activities were further categorized by intensity levels including walking or Tai chi (low intensity), bicycling or golf (moderate intensity) and swimming or jogging (high intensity). Participants who did other forms of physical activity that were not listed as examples were also collated and analyzed.
Operational definitions of sarcopenia Probable (EWGSOP2) or possible (AWGS 2019) sarcopenia is defined by low muscle strength (using handgrip or chair-stand test in EWGSOP2 and handgrip in AWGS 2019) or reduced physical performance (based on chair-stand test in AWGS 2019) [2,17]. A definitive diagnosis of sarcopenia is confirmed by presence of low muscle mass in participants meeting criteria for possible/probable sarcopenia. Aligning with AWGS 2019 criteria for confirmed sarcopenia, we included gait speed and SPPB in addition to chair-stand test amongst the physical performance measures.

Statistical analysis
Sample size was calculated using G*Power 3.1.9.4 [32,33]. We projected a sample size of 779 seniors for an 80% power with a 5% type 1 error rate to detect a Pearson's correlation coefficient as small as 0.10 between STS and grip strength performance.
Descriptive statistics used to summarize participant data were the mean, standard deviation, minimum and maximum values. Associations between skeletal mass index, strength and physical performance measures were examined using Pearson correlation coefficient. Two-way analysis of variance (ANOVA) was used to assess the main effects of gender and age on 30CST and 5TSTS performance. Chi square test of homogeneity was used to compare prevalence of sarcopenia diagnosed using different performance measures. To examine the physical construct underlying STS, we performed separate multiple linear regression for the outcomes of 30CST and 5TSTS, with strength (grip as a proxy), mobility (gait speed), endurance (6MWT) and balance (TUG) as independent variables, adjusted for age, gender, muscle mass, height and weight. All variables were entered simultaneously in multiple linear regression analysis incorporating the backward elimination variable selection approach, with statistical significance to enter/remove at P = 0.05/0.10. Statistical analyses were performed using IBM SPSS Statistics for Windows, version 25 (IBM Corp., Armonk, N.Y., USA).

Demographics and physical performance measures (Tables 1, 2)
Eight hundred and eighty-seven (887) participants completed baseline assessment, with mean age of 67.3 ± 7.0 years, and female predominance (72.9%). Performance on 30CST, 5TSTS, TUG, habitual gait speed and 6MWT was similar in men and women (p> 0.05). Mean grip strength was significantly higher in men (31.7 ± 7.0 kg vs 21.6 ± 4.4 kg, p< 0.01). We stratified STS performance by gender and age groups (51-60, 61-70 and 71+ years old) ( Table 2). While performance on both 30CST and   Physical fitness measures independently associated with STS (Table 5) Measures of functional fitness independently associated with 30CST performance included grip strength, TUG, habitual gait speed and 6MWT. With the exception of gait speed, these measures were also associated with 5TSTS performance. Weight and fat mass index significantly impacted both 30CSTand 5TSTS performance. Examination of the standardized coefficients revealed TUG to exhibit the greatest influence on 5TSTS performance (β = 0.504, p < 0.001), while 30CST performance was most strongly associated with 6MWT (β = 0.298, p < 0,001).

Discussion
Our findings suggest STS performance relates significantly to measures of grip strength, gait speed, endurance and balance. However, its weak correlation with grip strength suggests that the two measures are not equivalent strength test proxies of one another. We also build on existing sarcopenia literature, demonstrating muscle mass to be more strongly related to grip strength compared with a surrogate measure of lower body strength via STS. STS tests were more strongly correlated with gait speed, endurance and balance compared with grip strength, an observation consistent with the reported association between STS tests and fastest gait speed [34]. STS is a functional maneuver which not only involves knee extensor strength [35,36], but also trunk stability [37], sensation and balance [19]. Objective measures of lower extremity strength using isokinetic dynamometer have also been more strongly associated with customary gait speed compared with grip strength [38]. The generally weak correlation between grip strength and STS in our cohort is consistent with observed poor associations between objective measures of hand grip strength and knee extensor/flexor strength [38][39][40]. Caution is thus needed when using grip strength as a sole proxy measure for lower extremity strength or performance. Furthermore, a task such as STS obviously does not involve the muscles responsible for gripping, therefore the poor correlation between grip strength and STS performance should not come across as too surprising.
Muscle mass exhibited modest correlation with grip strength, and negligible association with lower limb strength as represented by STS tests. The dissociation between muscle mass and muscle strength with age has been previously described and attributed in part to intramuscular adiposity, shifting the attention towards muscle quality as a more clinically relevant determinant of physical performance in older adults [41,42]. In addition, age-related decline in muscle mass and strength of the lower body is also more pronounced than that of the upper body, owing to reduced physical activities such as walking, running and stair-climbing that would expectedly have a greater impact on the lower body, and compensatory upper body movements such as use of arm muscles in routine activities such as rising from a chair [43]. In addition, greater deficits of muscle power relative to mass and strength have been reported in older individuals [43,44]. The STS task has been used for measurement of muscle power, with demonstrated relationship to a spectrum of fitness measures [45]. The unexpected inverse correlation, albeit weakly, between STS performance and muscle mass may suggest reduced ability to fully recruit motor units for the force necessary to perform daily living tasks such as rising from a chair or stair climbing.
Although 30CST and 5TSTS were strongly correlated, their physical construct may not be identical. Both tests appear to be representative of muscle strength, being independently associated with grip strength. However,   while 5TSTS was particularly dependent on dynamic balance, cardiorespiratory endurance was a stronger determinant of performance on 30CST. The standardized time protocol of 30 s requires participants to have sufficient physical endurance for continued repetitions as opposed to just the pre-determined five repetitions in 5TSTS. This is reflected in the wide variability of performance on 30CST, ranging from 3 to 35 repetitions in our cohort. However, this could also be due to the large sample size where wide variability of 5TSTS and other physical tests could also be seen. Our findings parallel the observed poorer correlation between 5TSTS and pulmonary function, compared with 30CST, in patients with chronic obstructive pulmonary disease [46]. Higher body weight in obese individuals is known to impair weight bearing activities and reduce exercise capacity [47], accounting for the negative impact of body weight on 30CST performance. Both STS tests were influenced by dynamic balance, albeit more so for 5TSTS than 30CST, plausibly because the latter is more fatiguing [48] such that the effect of balance, which declines with lower limb muscle fatigue [49] may become less significant. The association of 5TSTS and 30CST with various measures of functional fitness supports STS tests in representation of overall physical performance as opposed to muscle strength in isolation and in tandem, its influence by body functions (such as cardiovascular and neural systems) beyond skeletal muscle. Generally, the FMI indices are lower in our cohort compared to other Asian populations, however the lower mean FMI values in females follow a similar trend [28]. Intriguingly, a higher FMI, not SMI, is significantly associated with poorer performance in the STS tests in both the univariate and multivariate models. This affirms previous literature that body fat or myosteatosis impairs muscle performance particularly in functional performance in STS tests and related lower limb physical assessments [16,50]. This also indicates that the STS test may be a reasonable proxy in the evaluation of muscle quality. More importantly, the results suggest that the deleterious impact of sarcopenia may not be solely due to the loss of muscle mass but also from a reduction in muscle quality from the negative biomechanical and inflammatory impact of fat accumulation [29]. Future research to confirm these findings could evaluate other domains of muscle quality in the community with advanced technology. These include non-invasive, portable modalities such as quantitative musculoskeletal ultrasound to evaluate muscle structure [51] and near infra-red spectroscopy (NIRS) to characterize muscle oxidative potential as a proxy for mitochondrial capacity [52]. Increasing age is also correlated with poorer STS test performance as it may represent progressive diminishing muscle quality over time [53].
The introduction of possible/ probable sarcopenia to diagnostic algorithms by EWGSOP2 and AWGS 2019 seeks to raise awareness of sarcopenia for early lifestyle intervention and timely evaluation. The criterion of weakness by grip strength and poor performance on STS likely identifies different populations of older persons as having possible/ probable sarcopenia, given similar prevalence when applying either measure in isolation but significantly higher prevalence with availability of either measure in the diagnostic algorithm. This is likely because STS tests are more representative of overall physical performance than just strength itself. Overall, prevalence of confirmed sarcopenia with muscle mass measured via BIA was three to five times lower than respective diagnoses of possible/ probable sarcopenia, reinforcing observations that the loss of strength with age far exceeds the decline in muscle mass [54]. The lower prevalence of confirmed sarcopenia with both STS measures compared with grip strength in our overall cohort parallels the findings of a Korean cohort [55]. Further research is needed to identify physical differences between seniors differentially identified as sarcopenic based on performance measure applied. This also implies that single measures should not be used to identify sarcopenia as individual tests vary in sensitivity and specificity depending on how sarcopenia is defined [56]. Composite measures should be used as different tests are complimentary in their ability to detect different components of physical performance, strength and muscle mass. For example, the use of the SPPB to screen for sarcopenia had lower sensitivity if it was used alone without measures of muscle mass [57].
The similar prevalence of possible and confirmed sarcopenia identified by 30CST and 5TSTS suggests utility of the former in sarcopenia diagnostic algorithm, overcoming the floor effect of 5TSTS in older adults [5] and potentially facilitating better quantification if used as biofeedback. However, normative values and cutoffs will need to be specifically developed for its use in sarcopenia. Further, the choice of functional measure for sarcopenia diagnosis should be guided by its prognostic value for relevant clinical outcomes [58] and responsiveness to intervention [38,59].
The strengths of this study include a well characterized cohort of community-dwelling older adults beyond the target sample size necessary for the primary aim, who completed a comprehensive battery of functional performance and objective muscle mass measures. However, several limitations are acknowledged. Our cohort of participants included only those who were ambulatory which may not be truly representative of all of the older adults living in the community. Older adults who may have health conditions which prevent them from travelling to the test centers are not represented in this study. The prevalence of sarcopenia within community dwelling older adults may therefore be under estimated. The exclusion of seniors who were residents of sheltered or nursing homes also limits generalizability of the findings. While upper limb strength was measured objectively using a dynamometer, we lacked comparative objective measure of lower limb strength.

Conclusion
STS tests in older adults are influenced by strength, dynamic balance and cardiorespiratory endurance, and thus represent overall physical performance rather than mere muscle strength. Because of this, it also identifies a different subset of the population with possible sarcopenia that may not have been picked up by hand dynamometer testing (grip strength). The utility of a multitest battery to assess sarcopenia will hence be more appropriate. Further research is needed to identify physical differences between seniors differentially identified as sarcopenic based on performance measure applied as subsequent diagnosis of confirmed sarcopenia is more prevalent with grip strength. Poor performance on STS may also be due to reduction in muscle quality rather than muscle mass. Further research to evaluate muscle quality in the community with advanced technology may provide a different perspective of the functional impact of sarcopenia beyond the traditionally described losses in muscle strength, performance or muscle mass.