Introduction

Sarcopenia is defined as a progressive muscle disorder prevalent among older adults. According to the updated operational definition of sarcopenia by the European Working Group on Sarcopenia in Older People (EWGSOP2) low muscle strength is suggested as a key characteristic of sarcopenia [1]. Detection of low muscle quantity and quality is used to confirm the sarcopenia diagnosis, and additionally, poor physical performance is indicative of severe sarcopenia [1]. The prevalence of sarcopenia varies across different population settings and ethnicities, according to the definitions, the diagnostic methods, and the cut-offs used [2]. Sarcopenia is a risk factor for falls, fractures, disability, dependency, poor quality of life, cognitive impairment, depression, institutionalization, hospitalization, and mortality [3-5]. Considering this, screening for sarcopenia in an early stage is important, because there is a possibility these adverse consequences to be prevented, delayed or sometimes even reversed with early, evidence-based interventions [1].

Nurses’ role in early detection of other geriatric health problems is well recognized in the literature. There is evidence that nurses in their daily practice with older adults are involved in cancer [6], frailty [7], delirium [8], falls [9], and nutritional screening [10]. However, the use of screening tools for sarcopenia by nurses is not well documented in the literature. Most studies on sarcopenia screening tools have not used nurses to validate the tools, although nurses are often the first point of contact for older adults or their families with nutritional or weight or muscle strength loss concerns.

The SARC-F is a widely used screening tool for sarcopenia. In view of its utility in everyday practice, SARC-F has been translated and validated in multiple different languages. Some researchers recommend the SARC-F in combination with the measurement of calf circumference (CC), SARC-Calf, as a screening tool for sarcopenia [11]. SARC-Calf seems a promising screening tool, as it demonstrates higher sensitivity than SARC-F itself [12-14]. The aim of this study is therefore to compare the validity of SARC-F and SARC-Calf screening tools for sarcopenia to be used by nurses in Greek older adults.

Methods

This is part of a larger multicenter study, in collaboration with the Hellenic Association of Gerontology and Geriatrics. The validity of the SARC-F and SARC-Calf tools was assessed in this part of the study, with a cross-sectional design, conducted between July 2020 and October 2022 (recruitment were temporarily paused due to Covid-19 restrictions) in a convenience sample of community-dwelling older adults living in Athens. Participants were recruited either as outpatients or their companions in a General Hospital in Athens or community settings and organizations, a choral group, or church.

Participants who met the following criteria were included; (1) aged 65 years or older; (2) able to walk but may use any aid; (3) able to communicate in Greek language; (4) willing to complete the survey; and (5) provided written consent to participate.

The exclusion criteria were individuals with the following conditions: (1) severe cognitive disorder, making difficult the communication or data collection; (2) an implanted pacemaker or defibrillator; (3) bedridden; (4) unable to communicate with the interviewer; (5) acute or chronic disease influencing the laboratory values, the response to the interview, or the ability to perform the required measurements. All the participants signed a written informed consent form. Participant information was collected through face-to-face interviews with a trained nurse, who was the main researcher of this study. The anthropometric measurements, muscle mass measurement, gait speed test, and handgrip strength test were also performed by the same trained nurse. The study protocol was approved by the Research Ethics Committee of the Nursing Department of the National and Kapodistrian University of Athens and the Scientific Council of the involved hospital.

The SARC-F questionnaire consists of 5 items: Strength, Assistance with walking, Rise from a chair, Climb stairs and fall. The scores range from 0 to 10, with 0 to 2 points for each item. A score equal to or greater than 4 is predictive of sarcopenia and poor outcomes [15]. For the translation and validation of SARC-F into Greek we followed the steps suggested in the methodological report by the European Geriatric Medicine Society (EUGMS) Special Interest Group (SIG) on Sarcopenia. According to this report a sample of between 50 and 100 community-living subjects aged 65 years or older should participate in the study of validation. The translation and cross-cultural adaption of SARC-F questionnaire into Greek has been described elsewhere [16].

Validation of the SARC-F questionnaire

Sensitivity, specificity, and positive and negative predictive values (PPV, NPV, respectively) of the SARC-F were assessed against four definitions of sarcopenia; EWGSOP2 [1], FNIH2 and FNH3 [17,18], IWGS [19]. Muscle strength was assessed by grip strength, which was measured using a digital handgrip dynamometer. Muscle mass was measured using bioelectrical impedance analysis (BIA) device (Tanita RD-545).

Appendicular skeletal muscle mass (ASM), equivalent to appendicular lean mass (ALM), was calculated using the following equation to obtain an ASM value closed to that measured by DXA: ASM/ht² (DXA) = 0.04^* BMI – 0.58Women +0.69^* ASM/ ht² (BMI = Body Mass Index) [20-21]. The physical performance was measured by the 4-m usual gait speed test. According to the EWGSOP2 criteria sarcopenia is confirmed when low muscle strength and mass are detected. Cut-off points for muscle strength by grip strength are < 27 kg and < 16 kg for men and women, respectively. Cut-off points for muscle mass are ASM/height² < 7 kg/h² for men and ASM/height² < 5.5 kg/h² for women. According to the FNIH criteria, the definition of sarcopenia depends either on two criteria (FNIH2; low muscle strength and mass) or on three criteria (FNIH3; slowness with low muscle strength and mass). Cut-off points for muscle strength by grip strength are < 26 kg and < 16 kg for men and women, respectively. Cut-off points for muscle mass are ASM/BMI < 0.789 for men and < 0.512 for women. Cutoff point for physical performance measured by gait speed is ≤ 0.8 m/s. According to the IWGS definition, sarcopenia is confirmed when both low muscle mass and low physical performance exist. Cut-off points for muscle mass are ASM/height² < 7.23 kg/h² for men and ASM/height² < 5.67 kg/h² for women. Cut-off point for physical performance measured by gait speed is < 1.0 m/s. Finally, the SARC-F was assessed against probable sarcopenia, which is based only on the detection of low muscle strength according to the EWGSOP2 criteria.

The SARC-Calf screening tool

Afterward, CC item was scored as 0 point if the CC was ≥ 31 cm and as 10 points if it was < 31 cm [22]. SARC-F was scored as described above. By adding CC score to the SARC-F score, the SARC-Calf variable was developed. A final score of 11 or more, was classified as risk for sarcopenia and score less than 11 was classified as no risk for sarcopenia [22]. SARC-Calf was assessed against the above-mentioned definitions of sarcopenia and against the probable sarcopenia.

Statistical Analysis

Demographic, anthropometric characteristics, and clinical features were presented using mean and standard deviation for continuous variables; frequency and percentage were reported for categorical variables.

The characteristics of patients were compared according to the cut-off point of the SARC-F and the P values were assessed using Student’s t-test for continuous variables with normal distribution, Mann–Whitney U test for continuous variables with asymmetric distribution and Pearson’s Chi-square test (or Fisher’s Exact test) for categorical variables. P value < 0.05 was considered statistically significant.

For the clinical validation of the SARC-F the difference of diagnosis between the SARC-F and the 4 operational definitions of sarcopenia was tested by a Pearson’s Chi-squared test. Finally, sensitivity, specificity, PPV, and NPV value of the SARC-F according to the 4 operational definitions of sarcopenia and the probable sarcopenia were assessed. Afterward, the same procedure was followed for the validation of the SARC-Calf. Statistical analyses were performed using SPSS 28.

Results

A total of 107 older adults were provided with the opportunity to participate in this study. One-hundred older adults (n = 100) accepted to participate (response rate 93.5%). Reason of refusal was psychological stress. The age range for all the participants was 65-91 years. The median age of the whole study population was 72.50 years old (standard deviation = 9), and 59 participants (59.0%) were women.

Clinical validation of the Greek SARC-F

Among the 100 individuals the SARC-F identified 19 (19.0%) at high risk for sarcopenia. The prevalence rate of sarcopenia based on the SARC-F was 6 (6.0%) men and 13 women (13.0%). Table 1 displays the average, baseline characteristics of the participants who were grouped according to their SARC-F scores. A total score of 4 points and greater was classified as having a high risk for sarcopenia. A statistically significant relationship was found between SARC-F score and number of medications/polypharmacy (p = 0.044, p = 0.037, respectively), CCI (p = 0.042), instability (p < 0.001), walking frequency (p = 0.008), and number of falls in the last year (p = 0.019). Moreover, a statistically significant relationship was found between SARC-F score and muscle strength (p = 0.016) and physical performance (p < 0.001). The participants in the SARC-F ≥ 4 group had a lower mean muscle strength and gait speed. Afterward, probable sarcopenia, as detected via muscle strength, was statistically significant associated with SARC-F (p = 0.008). Depending on the definition used, the prevalence of sarcopenia varied from 10.0% (EWGSOP2, FNIH3) to 37.0% (IWGS) (Table 2).

Table 1: Population characteristics based on the SARC-F questionnaire.

Table 2: Sarcopenia classification according to different definitions.

Table 3 summarizes the values of sensitivity, specificity, PPV, and NPV, for the SARC-F questionnaire, using EWGSOP2, FNIH2, FNIH3, and IWGS criteria consecutively as the reference standards. The sensitivity of this tool ranged from 27.0% (IWGS) to 50.0% (FNIH3) and the specificity from 82.2% (EWGSOP2) to 85.7% (IWGS). Furthermore, all the PPVs, which indicated the probability of presenting sarcopenia in case of a positive screening test, were always below 60.0%, with a minimum of 15.8% (EWGSOP2) and a maximum of 52.6% (IWGS). NPV values ranged between 66.7% (IWGS) to 93.8% (FNIH3) indicating a high probability of actually not presenting sarcopenia when the SARC-F is negative. Also, SARC-F was assessed against probable sarcopenia, indicating 42.1% sensitivity, 86.4% specificity, 42.1% PPV, and 86.4% NPV. 

Then, SARC-Calf was assessed against the same definitions of sarcopenia and its validity results were compared to SARC-F (Table 3).  Sensitivity was lower than that of SARC-F. Specificity was improved, ranging from 95.6 to 98.4%. PPV was much higher in all cases except for the FNIH3 definition. NPV was similar to that of SARC-F. The same findings regarding sensitivity, specificity, and NPV were found when SARC-Calf and SARC-F were compared against probable sarcopenia. However, PPV was similar to that of SARC-F.

Table 3: SARC-F and SARC-Calf validated against different sarcopenia definitions and probable sarcopenia.