SARC-F and SARC-Calf Tools for Nurses to Screen Sarcopenia in Older Adults

Purpose This study aimed to compare the validity of SARC-F and SARC-Calf screening tools for sarcopenia to be used by nurses in Greek older adults. Methods For the clinical validation of the Greek version of SARC-F, a cross-sectional study was conducted to assess sensitivity, specificity, positive and negative predictive values (PPV and NPV, respectively) of the SARC-F against 4 definitions of sarcopenia. The SARC-F questionnaire was combined with calf circumference. SARC-Calf was developed and assessed against the same definitions of sarcopenia. Results One hundred older adults, ≥ 65 years old, (median age 72.50 years old, standard deviation = 9), took part in the clinical validation of the Greek SARC-F and SARC-Calf. Based on the definition used for sarcopenia, sensitivity of SARC-F ranged from 27.0 to 50.0%, specificity from 82.2 to 85.7%, NPVs between 66.7 and 93.8%, and PPVs were always below 60.0%. The SARC-Calf demonstrated improved specificity (95.6 to 98.4%) but lower sensitivity (10.0 to 20.0%). Conclusions The Greek version of SARC-F appears to be a useful screening tool for nurses for precisely ruling out community-dwelling older adults without sarcopenia. Nurses could have an important role in the early detection of sarcopenia by implementing the SARC-F screening tool. Further research is needed to assess the SARC-Calf validity in more vulnerable populations.


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][4][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 Citation: Pana A, Sourtzi P, Kalokairinou A, Galanis P, Velonaki VS (2023) SARC-F and SARC-Calf tools for Nurses to Screen Sarcopenia in Older Adults.Int  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][13][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].
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/ht 2 (DXA) = 0.04 * BMI -0.58 Women +0.69 * ASM/ ht 2 (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/height 2 < 7 kg/h 2 for men and ASM/height 2 < 5.5 kg/h 2 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/height 2 < 7.23 kg/h 2 for men and ASM/height 2 < 5.67 kg/h 2 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 Citation: Pana A, Sourtzi P, Kalokairinou A, Galanis P, Velonaki VS (2023) SARC-F and SARC-Calf tools for Nurses to Screen Sarcopenia in Older Adults.Int J Nurs Health Care Res 6: 1453.DOI: 10.29011/2688-9501.1014533classified 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 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.
Citation: Pana A, Sourtzi P, Kalokairinou A, Galanis P, Velonaki VS (2023) SARC-F and SARC-Calf tools for Nurses to Screen Sarcopenia in Older Adults.Int J Nurs Health Care Res 6: 1453.DOI: 10.29011/2688-9501.1014533 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.

Discussion
In this study we carried out the validation of the SARC-F questionnaire into Greek according to the recommendations by EUGMS and we compared its validity with that of SARC-Calf.The results of the validation analysis indicated that SARC-F has a low sensitivity but a high specificity and high NPV.The PPV was low but even very good tests have poor PPV when applied to low-prevalence populations [23].These findings indicate that SARC-F is an appropriate tool for nurses for ruling out older adults without sarcopenia.This represents a positive property of a screening test, since when older adults score < 4 in SARC-F, it is considered strongly possible that they are no sarcopenic.Therefore, it eliminates the need for various cost and time-consuming device measurements such as muscle assessment by DXA or BIA and attributes to SARC-F the ability to be used as a feasible and suitable tool in community clinical settings.
The SARC-F has previously been validated into Greek by Tsekoura et al. [24].In that validation process the SARC-F questionnaire was assessed against only one definition (sensitivity 34.4%, specificity 93.2%, PPV 26.4%, and NPV 66.6%) and proved to be reliable on detecting with precision the absence of sarcopenia.These findings, except NPV, are in agreement with the findings of the present study.However, the present study enhances the validity of SARC-F since it is assessed additionally against three sarcopenia definitions.One more difference between the two studies is that the samples were recruited from different cities which may explain possible differences in sample characteristics.
Results regarding the validation of the SARC-F among community-dwelling older adults in other languages are similar, highlighting the low sensitivity and PPV, and the high specificity and NPV [25][26][27][28][29][30][31].The different validation results in other studies may be due to different methodology or sample characteristic.In the Romanian validation, older adults were recruited from nursing homes but there were strict inclusion criteria and were considered community-dwelling [32].The mean age of participants in the German (79.1 ± 5.2 years) and the Spanish (Spain) population (81.4 ± 5.9 years) was much higher than the present study [25,33].The findings of our study are consistent with these in a recent metaanalysis aiming at evaluating the diagnostic accuracy of SARC-F.Depending on the definition used, the sensitivity ranged from 27.0 to 77.0% and the specificity from 63.0 to 91.0% [34].The authors concluded that despite some limitations, the SARC-F because of the high practicability and specificity remains an effective screening tool for sarcopenia in the older population.
The findings of the present study revealed that SARC-F is superior to SARC-Calf regarding the sensitivity.However, SARC-Calf indicated higher specificity and PPV than SARC-F (except for FNIH3 definition) and similar NPV.Bahat et al. [22] found similar results when they compared SARC-F with SARC-Calf in a sample of Turkish population.On the other hand, other studies indicated improved sensitivity of SARC-Calf in comparison with SARC-F [12][13][14].The different prevalence of sarcopenia or the average age of the participants between these studies and our study may explain their improved, but not perfect sensitivity.The performance of SARC-Calf among other populations e.g., nursing home residents or other settings (e.g., hospitals), where the prevalence of sarcopenia is higher, remains to be further investigated.
Furthermore, in the present study, it was found that in the case of the SARC-F ≥ 4 group, muscle strength and physical performance, both basic components of sarcopenia, were statistically significant correlated, enhancing the value of SARC-F as a screening tool for sarcopenia.The risk of probable sarcopenia, assessed by muscle strength, was higher in the group of older adults with SARC-F score ≥ 4, highlighting the significant relationship between probable sarcopenia and SARC-F as screening tool for sarcopenia.There is also a statistically significant association between the SARC-F ≥ 4 group and the number of medications/ polypharmacy.This finding has been also indicated in a previous scoping review.According to this review, sarcopenia or risk for sarcopenia are associated with polypharmacy or the number of medications in community-dwelling older adults, regardless of diagnostic criteria used for sarcopenia [23].
The number of comorbidities, measured by CCI and the number of falls were statistically significant associated with SARC-F, indicating that older adults at risk for sarcopenia may have more than one chronic disease at the same time and higher risk for falls.Tan et al. [24] have also found that SARC-F is associated with higher CCI and higher number of falls in a sample of outpatients.Moreover, the statistically significant association found between SARC-F and instability may explain the higher risk for falls among older adults at risk for sarcopenia.The relationship between SARC-F and walking frequency was also investigated among community-dwelling older Brazilians during the pandemic COVID-19 [25].Their findings are in agreement with our study indicating that walking frequency (minutes/week) is low in participants with risk for sarcopenia [25].
The SARC-F administration and the assessment of sarcopenia in this study were performed by a trained nurse.The nurse characterized SARC-F as a quick and easy-to-use tool in community-dwelling older adults.The majority of the participants responded to the questions without any difficulty or reluctance.The nurses' vital role in the early detection of sarcopenia by implementing screening tools is not fully recognized in the existing literature [35].There are only a few studies that involve nurses in sarcopenia screening and most of them concern community or home care nurses [36][37][38][39][40].However, it is suggested that also hospitalbased nurses could contribute to the early detection of sarcopenia, recognizing possible signs of sarcopenia, and implementing screening tools [35].Compared to other health professionals, nurses work more next to the community-dwelling older adults as well as inpatients.Therefore, they may undertake autonomously the screening process of sarcopenia and refer the individuals at risk to the specialist members of the multidisciplinary team [35].
This study has some strengths and limitations.First, to our knowledge, this is the first study in Greece which attempted to compare the validity between SARC-F and SARC-Calf and to assess it against four currently agreed and commonly used definitions of sarcopenia.Secondly, this study attempted to highlight especially the role of nurses in screening of sarcopenia.On the other hand, we used a BIA device for the assessment of muscle mass, instead of more precise, but expensive and less convenient techniques; magnetic resonance imaging, computed tomography or DXA.Nevertheless, we used a BIA equation and BIA remains under some circumstances an acceptable method for the estimation of muscle mass [41].In addition, the measurement of CC may in some cases hide a possible sarcopenic obesity due to the intramuscular or subcutaneous adipose tissue deposition in obese subjects [12].Finally, we included a convenience sample of Greek older people of volunteers, which can limit the generalization of our results to other populations.

Conclusions
The Greek SARC-F demonstrates poor sensitivity, but high specificity and NPV, indicating that nurses can use it and detect with accuracy community-dwelling older adults without sarcopenia, independently of the diagnostic criteria used.The SARC-Calf indicated improved specificity but not sensitivity in comparison with SARC-F.Νurses can significantly contribute to the management of sarcopenia, through its early detection, by applying the SARC-F questionnaire.Further studies are needed to validate the SARC-Calf in different populations and settings with a higher prevalence of sarcopenia.Moreover, nurses may guide future health promotion interventions with content focusing on the prevention of sarcopenia and the identification of older adults at risk through the SARC-F administration.

Table 1 :
Population characteristics based on the SARC-F questionnaire.
*Percentages (%) are presented within gender.Statistically significant differences are marked in bold Abbreviations: EWGSOP2, the European Working Group on Sarcopenia in Older People 2; FNIH, the Foundation for the National Institutes of Health with 2 or 3 criteria, respectively; IWGS, the International Working Group on Sarcopenia

Table 2 :
Sarcopenia classification according to different definitions.

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