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INTRODUCTION

Diabetes mellitus (DM) is a chronic syndrome that is considered a public health problem in a number of countries, irrespective of their level of development, due to its impact on people’s lives.1 In 2021, the International Diabetes Federation2 estimated that around 10.50% of the world’s population aged 20 to 79 years (approximately 537 million people) live with diabetes. Currently, around 15.7 million Brazilians have DM, and this number is projected to reach 23.2 million by 2045.2

Chronic hyperglycemia, a result of uncontrolled type 2 DM (DM2), causes microcirculatory damage, impairing the function of various organs and tissues and predisposing patients to chronic complications from micro- and macrovascular injuries. These complications mainly manifest as retinopathy, nephropathy, neuropathy, peripheral arterial disease, and coronary disease.3 However, damage to skeletal muscles, such as accelerated decline in muscle quality and quantity, has also been described as a complication of diabetes.4

In 2010, the European Working Group on Sarcopenia in Older People (EWGSOP)5 defined sarcopenia as a progressive and generalized loss of muscle mass associated with a decline in performance and muscle strength. In 2018, the consensus was updated by the EWGSOP 2,6 in which sarcopenia was characterized as a muscle disease, with reduced muscle strength as the main determinant; sarcopenia can be suspected by the presence of this condition alone.

Several studies have evaluated the prevalence of sarcopenia in people with diabetes according to current diagnostic criteria. In Singapore, in association with the Asian Working Group for Sarcopenia, Fung et al.7 found a 27.4% prevalence among older diabetics aged 60 to 89 years. Using Foundation for the National Institutes of Health criteria in a sample of Brazilians aged > 50 years, Pechmann et al.8, found sarcopenia prevalences of 12.9% and 5.4% among DM2 patients and controls, respectively. In 2020, Freitas et al.9 assessed sarcopenia among older adults with DM according to EWGSOP and EWGSOP 2 criteria, finding prevalences of 16.9 and 7%, respectively.

Sarcopenia has been independently associated with many negative health outcomes, such as falls, increased risk of functional disability, lower quality of life, admission to long-term care facilities, hospitalization, and even death.10

The SARC F questionnaire (S – strength, A – assistance in walking, R – rising from a chair, C – climbing stairs, and F – falls) was developed in 2013 as the first simple and easyto-use screening tool to identify sarcopenia risk in clinical practice. It consists of 5 questions on: strength, assistance in walking, difficulty getting out of bed or a chair, difficulty climbing stairs, and history of falls.11 However, the SARC F has high specificity and low sensitivity, which is an important limitation, since sensitivity determines a test’s ability to correctly identify people with the disease.12 In 2016, Barbosa- Silva et al.13 proposed the SARC CalF, which added calf circumference to the SARC F questionnaire to increase the instrument’s sensitivity and enable sarcopenia risk monitoring in clinical practice.

Given the health problems that diabetes and sarcopenia can cause, especially among older adults, screening, diagnosis, and intervention should occur early to minimize negative effects, especially in the initial stage of sarcopenia. Thus, the SARC F and SARC CalF can help health professionals care for these patients. However, these instruments must be validated in different populations.

The objective of this study was to evaluate the diagnostic power of the SARC F and the SARC CalF as screening tools for sarcopenia risk in older adults with DM2.

METHODS

This cross-sectional study was conducted at the endocrinology outpatient clinic of the Hospital das Clínicas de Pernambuco; data were collected between July 2022 and February 2023.

A total of 138 older men and women diagnosed with DM2 were recruited. The exclusion criteria for this convenience sample were: decompensated chronic renal failure (serum creatinine ≥ 2.0 mg/dL), neuromuscular diseases, a previous history of stroke and motor sequelae, cognitive impairment that could prevent comprehension of the questions and/or communication with the researchers, active malignant neoplasm, body mass index ≥ 40 kg/m², or physical limitations that could prevent anthropometry and bioelectrical impedance testing. The final sample consisted of 128 participants who met the inclusion criteria: age 60 to 80 years and diagnosed with DM2 for > 12 months.

Anthropometric assessment included weight (kg), height (m), and calf circumference (cm). Calf circumference was determined with a measuring tape (1 mm accuracy) while the participant was seated with both feet on the floor. For all measurements (taken in duplicate), the participants were barefoot and wearing light clothing. If a measurement difference > 0.1 kg or 0.1 m occurred, a third measurement was taken and the average of the two closest measurements was used in the analysis. We used the cut-off points of Barbosa-Silva et al.13,14 to determine adequate calf circumference: > 33 cm for women and > 34 cm for men.

Body mass index was determined as weight/height2 and was classified according to Pan American Health Organization cut-off points.15

A Biodynamics BIA 310E bioimpedance body composition analyzer (Biodynamics, Seattle, WA, USA), was used for bioelectrical impedance testing. This device analyzes muscle mass using an equation with resistance and reactance values. Skeletal muscle mass was calculated using an equation by Janssen et al.16, and the skeletal muscle mass index was determined using the following formula: skeletal muscle mass/ height². Appendicular skeletal muscle mass was calculated according to a formula by Sergi et al.17, and the appendicular skeletal muscle mass index was determined using the formula: appendicular skeletal muscle mass/height ².

Muscle strength was assessed as handgrip strength using a Saehan model SH5001 manual dynamometer (Saehan, Seoul, Korea). The dynamometer was calibrated prior to data collection. Handgrip strength was measured 3 times, and the average of the highest 2 measurements was used in the analysis.

Physical performance was determined through a gait speed test. The participants were instructed to walk in a straight line for 4 meters at their usual pace. The average of 2 round trips was used to calculate gait speed (distance covered/time taken to complete the course). Time was measured in thousandths of a second using a stopwatch. All cut-off points used in this study are described in Box 1.

The SARC F and SARC CalF instruments were used to assess the risk of sarcopenia. The SARC F includes 5 domains:

1. 1. muscle strength
2. 2. the need for assistance in walking
3. 3. the ability to get up from a chair
4. 4. the ability to climb stairs
5. 5. the frequency of falls.

Each item was scored from 0 to 2 points, with a maximum score of 10 points. Participants scoring ≥ 4 points were considered at risk of sarcopenia.

The SARC CalF includes all 5 items on the SARC F (with the same score) plus CC, which is scored 0 if > 34 cm for men and > 33 cm for women, and 10 if ≤ 34 cm for men and ≤ 33 cm for women. Total SARC CalF scores ≥ 11 indicate a possible risk of sarcopenia.

Two sets of criteria were used to diagnose sarcopenia: EWGSOP, published in 2010, and the EWGSOP 2, published in 2018. According to the EWGSOP, sarcopenia is defined as low muscle mass associated with low muscle strength and/or low physical performance. According to the EWGSOP 2, sarcopenia is defined as low muscle strength associated with low muscle mass; when combined with low physical performance, it is considered severe sarcopenia.

Data on demographic (age, sex, race, and education) and clinical (comorbidities and disease duration) variables were collected through interviews conducted by the researchers.

The assessments were carried out in a single session, before or after pre-scheduled outpatient medical care, and were conducted by two interviewers, both of whom were nutritionists who had undergone prior training to administer the questionnaires and the electrical bioimpedance, handgrip strength, and gait speed tests.

The study was approved by the research ethics committees of the Federal University of Pernambuco (No. 5,517,887/CAAE: 53329721.2.0000.5208) and the Hospital das Clínicas da Pernambuco (No. 5,551,658/CAAE: 53329721.2.3002.8807). After the study’s objectives and methods had been explained to them, the participants provided written informed consent to participate.

IBM SPSS Statistics 25.0 (IBM, Armonk, NY, USA) was used for the statistical analysis. The normality of continuous variables was determined with the Kolmogorov-Smirnov test, and those with normal distribution were presented as mean and SD. Continuous variables with non-normal distribution are presented as median and IQR (P25 and P75). Student’s t-test and the Mann Whitney U test were used to compare continuous variables with normal and non-normal distribution, respectively.

Categorical variables were presented as frequencies and percentages, and the χ² and Fisher’s exact test (when applicable) were used to determine the associations between variables. The prevalence ratio was used to evaluate potential protective and risk variables.

The diagnostic power of the SARC F and SARC CalF was evaluated through sensitivity, specificity, and positive and negative predictive values. Sensitivity indicates the probability of correctly identifying individuals with sarcopenia, whereas specificity is the probability of correctly identifying individuals without sarcopenia. Positive predictive value measures the probability of having sarcopenia, while negative predictive value measures the probability of not having sarcopenia. A higher positive predictive value (fewer false positives) indicates a more specific test, while a higher negative predictive value (fewer false negatives) indicates a more sensitive test.

The diagnostic accuracy of the investigation methods was determined through ROC curve and AUC analysis. The AUC of the instruments was compared using the DeLong method.18 P < 0.05 was considered significant.

RESULTS

A total of 128 older adults were included, of whom 90 (70.30%) were women and 38 (29.70%) were men. Their mean age was 67.37 (SD, 5.3) years. Overall, the mean age of the men was higher than the women (68.74 vs 66.80 years), although not significantly so (p = 0.09). There were no significant differences between men and women regarding sociodemographic data, as shown in Table 1A. As expected, the men had a higher appendicular skeletal muscle mass index (p = 0.005), skeletal muscle mass index (p < 0.001), and handgrip strength (p < 0.001), and the women had lower gait speed (p = 0.004) (Table 1B).

According to EWGSOP and EWGSOP 2 criteria, the prevalence of sarcopenia was 25.00% and 10.90%, respectively. In both sets of criteria, the prevalence differed according to sex, being higher among men for the EWGSOP (p = 0.001) and higher among women for the EWGSOP 2 (although not significantly so).

The risk of sarcopenia according to the SARC F and SARC CalF was 17.20% and 23.40%, respectively. In both sets of criteria, the prevalence was higher in women, but not significantly so. In the EWGSOP, sarcopenia risk is based on low muscle mass, which is reflected in the skeletal muscle mass index. Low muscle mass was found in 29.70% of the participants and was more prevalent in men (p = 0.001). However, in the EWGSOP 2, sarcopenia risk is based on low muscle strength, which is measured through handgrip strength. Low muscle strength was found in 28.20% of participants. Table 2 describes and comparatively analyzes individuals considered at risk of sarcopenia according to the SARC F and SARC CalF, as well as those diagnosed with sarcopenia according to EWGSOP and EWGSOP 2 criteria.

Table 3 shows the results of the sensitivity/specificity analysis, positive predictive value, negative predictive value, and AUC for the SARC F and SARC CalF in comparison with the diagnostic criteria for sarcopenia and probable sarcopenia (low muscle mass [EWGSOP] and low muscle strength [EWGSOP 2]). For the SARC F, sensitivity varied between 12.55% (95% CI, 3.55–29.12) and 36.11% (95% CI 20.81–53.79) and specificity varied between 71.87% (95% CI 61.85–80.63) and 92.39% (95% CI 84.91–96.90). For the SARC CalF, sensitivity varied between 47.22% (95% CI 30.40–64.55) and 85.71% (95% CI 57.22–98.23) and specificity varied between 82.46% (95% CI 74.24–88.90) and 88.89% (95% CI 80.50–94.55).

Both instruments presented relatively high negative predictive values. For example, when compared according to EWGSOP 2 criteria, the negative predictive value of the SARC CalF was 97.94% (95% CI 92.89–99.41) and that of the SARC F was 91.72% (95% CI 88.10–94.20). This means that if the test result was negative for sarcopenia, the chance that the person actually did not have sarcopenia was 97.94 and 91.72% for the SARC CalF and SARC F, respectively.

The SARC CalF had higher ROC curve values than the SARC F. According to EWGSOP 2 criteria, the AUC of the SARC CalF and SARC F was 0.86 (95% CI 0.78–0.91) and 0.62 (95% CI 0.53–0.70), respectively; there was a significant difference between the curves (p < 0.001). Similar results were found for the EWGSOP criteria (p = 0.009). The AUC of the SARC CalF was higher for both low muscle mass (p = 0.32) and low muscle strength (p = 0.54) than the SARC F, but not significantly so. All ROC curves for the SARC-F and SARC-CalF are compared with reference diagnostic methods in Figure 1.

DISCUSSION

Among older adults with DM2, this study found a sarcopenia prevalence of 25% and 10.9% according to EWGSOP and EWGSOP 2 criteria, respectively. This variation can be explained by the fact that low muscle mass is the main diagnostic criterion for sarcopenia in the EWGSOP, whereas low muscle strength is used in the EWGSOP 2.

Another important to consider is the change in cut-off points used to assess muscle mass and strength, since both were lowered in EWGSOP 2. These results corroborate the findings of Freitas et al.9 in a population of older Brazilians diagnosed with DM2: the prevalence of sarcopenia according to EWGSOP (16.9%) criteria was more than double that of EWGSOP 2 (7%).

In older adults, sarcopenia is associated with frailty syndrome and unfavorable health outcomes, including physical disability, low quality of life, risk of institutionalization, and even death. Therefore, this population should be routinely screened for sarcopenia and, in positive cases, additional diagnostic tests should be performed.19 However, to diagnose sarcopenia skeletal muscle mass must be determined through computed tomography, magnetic resonance imaging, dual energy X-ray absorptiometry, or bioelectrical impedance testing. Muscle strength (using a dynamometer) and physical performance must also be determined, which makes diagnosis expensive, time-consuming, and less accessible, especially in public health units.

Although the SARC F questionnaire is a quick and easy method of screening for sarcopenia risk, studies have reported that the instrument has high specificity and low sensitivity. For example, when validating the SARC F as a screening tool for sarcopenia in a Hong Kong community, using different reference criteria to diagnose sarcopenia, Woo et al.12 found a specificity of 94.4% and a sensitivity of 9.9%. The instrument’s low sensitivity limits its applicability due to the high possibility of not detecting individuals with sarcopenia. On the other hand, its high specificity indicates that it correctly identifies people who do not have the condition, ie, if a patient is not at risk according to the SARC F, a diagnosis of sarcopenia can be discarded without further testing.20

Calf circumference has consistently been associated with favorable or unfavorable health outcomes, especially in older adults. Grigol et al.21 evaluated survival among nonagenarians and centenarians, finding that calf circumference was the only anthropometric variable significantly associated with mortality. With each additional centimeter of calf circumference, there was a 9% reduction in mortality risk for each month of follow-up. In our study, calf circumference was the most closely associated variable with sarcopenia, regardless of the reference standard. Thus, it can be considered a risk factor for sarcopenia. Kawakami et al.22 found a positive correlation between calf circumference and muscle mass, indicating that it could be an alternative means of assessing muscle mass for sarcopenia diagnosis; the suggested cut-off values for predicting low muscle mass were < 34 cm for men and < 33 cm for women.

Barbosa-Silva et al.10 suggested adding calf circumference to the SARC F questionnaire, which then became known as SARC-CalF. Barbosa-Silva et al.13 evaluated 179 older Brazilians, reporting that when using EWGSOP criteria to diagnose sarcopenia, the sensitivity of the SARC CalF and SARC F was 66.7% and 33.3%, respectively. Likewise, in our study, for all reference criteria the SARC CalF was more sensitive than the SARC F for predicting sarcopenia risk in older adults with diabetes.

Other studies have compared the diagnostic power of the SARC CalF and SARC F regarding sarcopenia risk. Tsuji et al.23 assessed 172 older adults with chronic muscle pain in Japan and found that the SARC-CalF had better sensitivity than the SARC F, although the specificity of both instruments was similar. Luz et al.24 found similar results in older Brazilians with Parkinson’s disease, ie, the SARC-CalF was more sensitive than the SARC-F, except at diagnosing low muscle mass.

An important result of this study was that sarcopenia was significantly more frequent among women than men according to EWGSOP criteria, indicating that sex can affect the prevalence of sarcopenia and low muscle mass, the main diagnostic criterion for sarcopenia according to the consensus. Some studies25,26 have reported that sex and age can also affect the screening capacity of the SARC F and SARC CalF. This could be due to the fact that, when answering questions about physical performance, men tend to overestimate their physical ability, unlike women, who may underestimate it. Xu et al.26 applied the SARC F and SARC CalF to older adults with DM2 in China, finding higher scores among women than men. However, in determining the risk of sarcopenia with these instruments, we found higher, but not significantly higher, scores among women. This divergence may be attributable to demographic and clinical variables between populations, given that Xu et al.26 evaluated hospitalized patients in China and we evaluated outpatients in Brazil.

Generally, an AUC of 0.5-0.7 indicates low accuracy, 0.7-0.9 indicates moderate accuracy, and > 0.9 indicates high accuracy.27 In all 4 analyzed criteria, the AUC was higher for the SARC CalF than the SARC F. However, although the AUC of the SARC CalF was greater than that of the SARC F, its accuracy is in the low-to-moderate range. These findings demonstrate that, although the SARC CalF has better diagnostic power than the SARC F, it is still imperfect. However, calf circumference can also be influenced by the amount of adipose tissue, as well as the presence of edema, which can mask sarcopenia in some individuals.28

In 2019, Kurita et al.29 added 2 variables to the SARC F that are associated with an increased risk of sarcopenia: age ≥ 75 years and BMI ≤ 21 kg/m². This new version was called the SARC F + EBM (E for elderly, and BM for body mass index). The validation study investigated 959 Japanese patients hospitalized with musculoskeletal disease, finding greater sensitivity than the SARC-F (77.8 vs 41.7%, respectively), as well as a higher AUC (0.82 vs 0.56, respectively). However, further research should compare and determine the validity of new instruments with better diagnostic sensitivity for sarcopenia in older adults with DM2.

This study involves certain limitations. Due to its cross-sectional design, causality could not be determined. Regarding bioelectrical impedance, which was used to assess body composition, most of the equations were developed and validated for healthy, non-obese individuals and have not been validated in clinical situations, so the assessment was an estimate.

CONCLUSIONS

Regardless of the reference criteria, the SARC-CalF had better sensitivity and diagnostic performance than the SARC-F. Therefore, the SARC-CalF seems to be the most appropriate tool for sarcopenia risk screening, and it can be a practical and simple alternative for health professionals to investigate signs and symptoms in clinical practice and help prevent sarcopenia among older outpatients with diabetes.

ACKNOWLEDGEMENTS

The authors would like to thank the staff of the Hospital das Clínicas endocrinology outpatient clinic, especially nutritionist Nathalia Karolyne de Andrade Silva, for her important contribution to the interview and data collection process.

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Notes

Author notes

Correspondence data Ilma Kruze Grande de Arruda – Universidade Federal de Pernambuco, Health Sciences Center, Department of Nutrition, Campus Universitário, Cidade Universitária – CEP: 50670-901 – Recife (PE), Brasil. E-mail: ilma.arruda@ufpe.br

Conflict of interest declaration

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