Introduction
The prevalence of diabetes in the US is steadily increasing, reaching 26.8% (14% in men and 12% in women) among adults aged 65 years or older [
1]. The estimated global diabetes prevalence is 19.3%, with North America and the Caribbean possessing the highest regional diabetes prevalence of 27% [
2]. Type 2 diabetes mellitus (T2DM) is associated with an accelerated reduction in muscle mass [
3], strength [
4] function [
5], disability [
6] and frailty [
7], resulting in reduced autonomy and an increased burden on public health care systems [
8].
Sarcopenia, characterized by a progressive loss of skeletal muscle mass, strength, and functional abilities [
9] is a common complication in older patients with T2DM [
10,
11], further increasing their risk for functional decline [
12], and physical disability [
13]. Compared to the general older population, studies evaluating sarcopenia in older T2DM patients are scarce with prevalence rates varying greatly, ranging from 7 to 29.3% [
14]. This disparity is attributed mainly to variations between populations, variations in quantitative evaluation methods, as well as different diagnostic criteria [
14,
15].
The European Working Group on Sarcopenia in Older People (EWGSOP2) recently updated its original algorithm for “sarcopenia case-finding”. Muscle strength rather than muscle mass has become the main criteria for diagnosis termed “probable sarcopenia” as muscle strength is the most reliable measure of muscle function [
16]. Sarcopenia is further confirmed by the additional detection of a low muscle mass measurement. The EWGSOP advises the use of either the chair rise test, but preferably the use of a handgrip strength test (HGS), due to it its association with functional limitations, and ease of administration in clinical settings.
Older patients with T2DM typically experience a significant loss of lower body strength [
17‐
19] which is associated with a deteriorating health status [
20], impaired mobility [
21] and loss of autonomy [
22]. Isometric knee extension strength testing (KES) using a relatively inexpensive hand-held dynamometer has been found to be valid and reliable in assessing lower body muscle strength with a moderate to high correlation to isokinetic measurements (considered to be the gold standard method) [
23‐
25],especially in older populations [
26]. Furthermore, KES has been found to be superior to HGS as an indicator of muscle dysfunction in patients with T2DM [
27]. Due to the increased adiposity often accompanying T2DM older patients, it is recommended that knee extension strength relative to bodyweight should be measured as it better relates to low mobility than absolute strength scores [
28].
Due to the importance in the early detection and treatment of probable [
29] and confirmed sarcopenia, we aim to identify the most appropriate screening strength test by comparing the prevalence of sarcopenia by the use of relative KES to absolute HGS measurements in older patients with T2DM. To this end, we evaluated the association between KES and HGS to appendicular skeletal mass index (ASMI), and the prevalence of low-test scores of sarcopenia parameters and common physical performance screening tests.
Discussion
The main finding of our study was that cut-off points for low KES identified considerably more patients with probable and confirmed sarcopenia compared to HGS testing using the EWGSOP2 cut-off points for low HGS. The low prevalence of sarcopenia using HGS cut-off points in older adults with T2DM found in our study (3%) was also observed by Villani et al. [
37] identifying 2.3% of his T2DM older patients with confirmed sarcopenia (age eligibility ≥50 years) and Freitas’s et al. [
38] identifying a somewhat higher prevalence rate of confirmed sarcopenia (7%) and mostly women (88%), potentially due to a higher ASMI cut-off point for women (6.0 kg/m2). This observation is perplexing since T2DM older patients are known to possess markedly reduced muscle strength [
5], and in particular low handgrip strength [
39], with an increased risk for sarcopenia [
40,
41].
Despite the EWGSOP2 algorithm’s potential to reduce health costs by reducing the number of DXA measurements to identify sarcopenic patients [
42], it has been often scrutinized by investigators, observing a markedly lower prevalence of probable and confirmed sarcopenia compared to the earlier EWGSOP1 guidelines. This lower prevalence of sarcopenia is mainly due to the reduced cut-off points for both HGS (3 k
“g and a 4 k
”g reduction in HGS for men and women respectively), and ASMI (a 0.25 kg/m
2 and 0.17 kg/m
2 reductions in men and women respectively [
42‐
45]. Indeed, in our cohort of older T2DM patients, a higher prevalence of mostly pre-sarcopenia (10%) and confirmed sarcopenia (4%) was identified using the EWGSOP1 cut-off points for low HGS.
The EWGSOP2 recommends the use of one or two strength tests as their primary criterion for the identification of sarcopenia, an upper body test (HGS) and a lower body test (five-repetition chair stands) [
16]. We believe that the addition of a lower body strength test to the HGS test is imperative since the HGS is a poor predictor of both total body strength [
20], and functional performance [
46,
47], while yielding dissimilar sarcopenia rates compared to lower body testing (chair stands), in a community-dwelling group of middle aged and older adults [
48]. The KES test can be recommended as an alternative lower body strength test for the chair rise test, as it involves less complex weight-bearing body movements [
49], is better suited for diabetics with peripheral neuropathy [
50], as well as obese older adults with moderate to advanced osteoarthritis [
51,
52].
Our study was not exclusive in observing that the identification of probable sarcopenia is dependent on the strength tests performed. Wearing et al. has shown that by choosing a proper strength screening test 27% of patients would benefit from the continuation of the screening process, possibly preventing further strength reductions through an early initiation of suitable interventions [
29]. The higher prevalence of probable sarcopenia in measures other than HGS was found in other studies using the new EWGSOP2 algorithm. Higher rates of probable sarcopenia using the chair rise test were found by Kim et (13% in women) [
53], as well as Johansson et al. (4.4% vs 1.3%) [
48], noticing that subjects identified with probable sarcopenia by chair raise, were heavier and more obese than subjects identified by HGS, probably due to the greater influence of relative leg muscle strength. Dodd et al. observed that chair rise detected double the prevalence rates of probable sarcopenia in comparison to the HGS (15% vs 7%), stating the need to perform both tests to better assess probable sarcopenia [
54].
The correlation found between KES and ASMI along with other body size measures (BMI, body weight, WC) is important as it can be associated with an “obesity paradox”. The obesity paradox is generally referring to the protective effect obesity imparts on decreased mortality in older adults [
55]. That said, the term obesity paradox has also been related to the added muscle mass [
11,
56] and muscle strength [
57], Caused by the anabolic effect that occurs through continuously carrying the added body mass associated with obesity. This phenomenon is especially expressed in the lower body [
58], through an increase in absolute KES [
59], underscoring the need to normalize KES to body size using relative strength cut-off points. Relative muscle strength (muscle strength divided by bodyweight) better identifies individuals with reduced muscle strength through either HGS [
60,
61] or KES testing [
28,
62], thus possibly reducing false negative sarcopenia assessments.
The high prevalence of obesity in our cohort, can possibly explain the low prevalence of confirmed sarcopenia through low ASMI scores that coincide with the higher BMI values generally associated with higher fat free mass [
63].
Overall, the prevalence of common health complications exhibited by the subjects in our study was somewhat lower than values generally seen in older T2DM patients [
64]. Our finding that muscle strength (both HGS and KES) was significantly correlated to duration of T2DM is in line with chen et al. [
62], while unlike Izzo et al. [
14], stating that diabetes duration does not increase the prevalence of sarcopenia. The finding that most of the patients possessing low physical performance scores, concurrently possess low relative KES compared to those with impaired HGS, further affirms the added value in using KES as a sarcopenia screening tool.
Our study has several limitations. Its main limitation is the relatively small sample of T2DM patients making our findings difficult to generalize to older adults with T2DM. Additionally, the majority of our patients were younger than 75 years of age with only a small number of patients being older than 75, thus reducing the potential to truly investigate the age factor on outcome measures.
Conclusion
In a cohort of 100 mostly obese T2DM older patients, relative KES cut-off points using a simple hand-held dynamometer can assist in the identification of mostly probable sarcopenia and confirmed sarcopenia cases using EWGSOP2 cut off points for low muscle mass. Using the EWGSOP2 cut off points for low muscle strength by HGS mostly failed to identify probable and confirmed sarcopenia, possibly due to high prevalence of normal absolute handgrip and ASMI values associated with subjects possessing high BMI and body weight.
It must be stated that our study is the first to assess the prevalence of probable and confirmed sarcopenia in older T2DM patients by relative KES cut off points. Due to the importance of the initial screening strength test for further analysis and early treatment of sarcopenia and to reduce false negative sarcopenia, it would be prudent to add a lower body strength test such as the relative KES while screening older T2DM patients for sarcopenia while using the EWGSOP2 guidelines.
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