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2023 - Comparison of Four Screening Methods For Sarcopenia Among Community-Dwelling Older Adults A Diagnostic Accuracy Study
2023 - Comparison of Four Screening Methods For Sarcopenia Among Community-Dwelling Older Adults A Diagnostic Accuracy Study
Geriatric Nursing
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A R T I C L E I N F O A B S T R A C T
Article history: This study aimed to compare the diagnostic values of SARC-F (strength, assistance with walking, rising from a
Received 10 August 2022 chair, climbing stairs, and falls), SARC-Calf (SARC-F combined with calf circumference), CC (calf circumfer-
Received in revised form 7 December 2022 ence), and the Yubi-wakka (finger-ring) test for screening for sarcopenia in community-dwelling older
Accepted 7 December 2022
adults. The Asian Working Group for Sarcopenia (AWGS) 2019 criteria were used as a standard reference. A
Available online 19 December 2022
total of 209 participants were enrolled, and 40.7% were identified as sarcopenia. The sensitivity, specificity,
and AUC were respectively 54.1%, 70.2%, and 0.687 for SARC-F; 76.5%, 73.4% and 0.832 for SARC-calf, 86.7%,
Keywords:
82.4%, and 0.906 for CC in men, and 85.5%, 63.3%, and 0.877 for CC in women. Relative to the “bigger,” a sig-
Calf circumference
Sarcopenia
nificant association between sarcopenia and the Yubi-wakka test (“just fits” OR: 4.1, 95% CI: 1.57 10.98;
SARC-F “small” OR: 27.5, 95% CI: 10.14 74.55) was observed. The overall accuracy of CC was better than SARC-Calf
SARC-Calf for sarcopenia screening.
Yubi-wakka (finger-ring) test © 2022 Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.gerinurse.2022.12.007
0197-4572/$ see front matter © 2022 Elsevier Inc. All rights reserved.
158 Y.-H. Lin et al. / Geriatric Nursing 49 (2023) 157 163
The diagnostic instruments for measuring muscle mass include or unable = 2); rise from a chair, how much difficulty do you have trans-
CT, MRI, and DEX.9 Although these three measurements are relatively ferring from a chair or bed (none = 0; some = 1; a lot or unable without
accurate, they are expensive. Another commonly used diagnostic help = 2); climb stairs, how much difficulty do you have climbing a flight
method is bioelectrical impedance analysis (BIA), which is technically of 10 stairs (none = 0; some = 1; a lot or unable = 2); falls, how many
challenging and may not be readily accessible.16,17 Therefore, finding times have you fallen in the past year (none = 0; 1 3 falls = 1; 4
simple, fast, and reliable screening tools is imperative. falls = 2)” (P. 631).25 Scores range from 0 to 10; a total score higher
Existing screening tools include the SARC-F (strength, assistance than 4 is considered as having sarcopenia. The SARC-F has a sensitiv-
with walking, rising from a chair, climbing stairs, and falls),18 SARC- ity, specificity, and AUC of 3.8-9.9%, 94.2-99.1%, and 0.78-0.9,
Calf (SARC-F combined with calf circumference) test,19 calf circumfer- respectively.25
ence (CC),20 Yubi-wakka (finger ring) test,21 MSRA-5 and -7 (Mini
Sarcopenia Risk Assessment)22 and Ishii test.23 In 2019, the AWGS24
recommended the use of SARC-F,18 SARC-Calf,19 and CC20 as primary SARC-Calf
screening tools for sarcopenia. However, the validity of these tools
has not been tested in Taiwan. An alternative is the Yubi-wakka (fin- The SARC-Calf questionnaire was developed by Barbosa-Silva et
ger-ring) test,21 which is a simple, convenient, and fast self-screening al.19 in Brazil. It improved the sensitivity of SARC-F by adding the CC
method that does not require professional assistance. measurement. Scores are computed as SARC-F score plus an addi-
The purpose of this study is to compare the validity of SARC-F,18 tional value based on CC, with CC in females > 33 cm = 0 and 33
SARC-Calf,19 CC,20 and Yubi-wakka (finger-ring)21 test for sarcopenia cm = 10, and CC in males > 34 cm = 0 and 34 cm = 10. The total
screening among community-dwelling older adults to find suitable score ranges from 0 to 20, with a score 11 suggestive of sarcopenia.
sarcopenia screening tools, specifically for the community of Taiwan, SARC-Calf has a sensitivity, specificity, and AUC of 66.7%, 82.9%, and
to enable the early detection of sarcopenia and allow for the timely 0.736, respectively.19
implementation of preventive intervention to reduce the threat of
disability and improve the quality of life.
Calf circumference (CC)
Methods
Kawakami et al.20 designed the CC measurement in Japan as a
marker for muscle mass. The CC is measured to the nearest 0.1 cm
Study design and population
with the patient in a standing position using a non-elastic tape mea-
sure. The tape measure is placed around the calf without putting
We conducted a diagnostic accuracy cross-sectional study to
pressure on the subcutaneous tissue and is moved along the length
examine the psychometric properties of four screening tools. During
of the calf to obtain the maximum circumference. The average of two
October and November 2020, we used continuous purposive sam-
CC measurements for each leg was recorded, and these values were
pling to recruit older adults dwelling in the Mailiao community in
averaged again over both legs for the final value. The cut-off values
Yunlin City, Taiwan. Participants over 65 years of age and who could
for predicting sarcopenia from CC measurements were 34 cm in men
communicate with each other were included in this study. The exclu-
(AUC 0.94, sensitivity 88%, specificity 91%) and 33 cm in women (AUC
sion criteria were: (1) physical and/or mental incapacity to perform
0.84, sensitivity 76%, specificity 73%).20
requested assessments, such as being bedridden or at the end of life,
severe dementia, or being unable to walk independently; (2) contra-
indications for BIA, such as having a pacemaker or implanted Yubi-wakka (finger ring) test
electronic device; (3) presence of factors affecting the accuracy
of CC measurement and finger ring test, such as clinically visible Tanaka et al.21 developed a simple self-screening method in Japan.
lower extremity edema. The finger ring test uses the ring circumference formed by the thumb
and index finger of both hands to evaluate whether the circumfer-
Research ethics ence of the calf is larger than the circumference of the fingers. The
evaluation results are divided into three categories: (1) “bigger”
The study protocol was approved by the Research Ethics Commit- refers to the calf being bigger than the finger ring, indicating the ring
tee of China Medical University (CRREC-109-133), who also autho- cannot be closed; (2) “just fits” refers to the calf and finger ring being
rized a waiver of written informed consent for the participants. about the same size; and (3) “smaller” refers to the calf being smaller
Participant information was collected through personal interviews than the finger ring, creating a gap. “Just fits” and “smaller” indicate a
with the primary researcher (Ya-Huang Lin). risk of developing sarcopenia.21
Relative to the “bigger” group, community-dwelling older adults
Assessment of sarcopenia using AWGS criteria in the “just fits” and the “smaller” groups were found to be associated
with sarcopenia (“just fits” OR: 2.4, 95% CI: 1.4 4.1 and “smaller” OR:
We used the AWGS 2019 criteria as the standard reference for 6.6, 95% CI: 3.5 13) by multivariate analyses.21
the diagnosis of sarcopenia. The detailed criteria are: (1) muscle
mass < 7.0 kg/m2 for men, < 5.7 kg/m2 for women; (2) grip strength
< 28 kg for men, < 18 kg for women; and (3) gait speed for a 6-meter Anthropometric measurement
walk < 1.0 m/s.
We used a BIA device (Inbody 270; Biospace, Seoul, Korea) to
SARC-F measure appendicular skeletal muscle mass (ASM) and body fat
mass. During the measurement, participants were asked to stand
The SARC-F questionnaire was developed by Malmstrom et al. with their feet in firm contact with the electrodes at the front and
(2013)18 in the United States. It assesses five components: “Strength, back of their foot and to grip an electrode in each hand so that the
how much difficulty do you have in lifting and carrying 10 lb. (None = 0; palms and thumbs were in complete contact with it. The ASM refers
Some = 1; A lot or unable =2); assistance in walking, how much difficulty to the sum of skeletal muscle masses of the four limbs. The skeletal
do you have walking across a room (none = 0; some = 1; a lot, use aids, muscle index (SMI) was calculated as ASM/height (kg/m2).24,26
Y.-H. Lin et al. / Geriatric Nursing 49 (2023) 157 163 159
Fig 1. The ROC curves of SARC-F, and SARC-Calf against the AWGS criteria in total study populations (A), men (B) and women (C).
and an AUC of 0.877 (95% CI: 0.819 0.935) (Fig. 2), with a sensitiv- Discussion
ity and specificity of 85.5% and 63.6%, respectively, in women
(Table 2). This study evaluated SARC-F, SARC-Calf, CC, and the Yubi-wakka
(finger-ring) test as screening tools for sarcopenia using the AWGS
2019 consensus as the diagnostic criteria. The results showed that
Yubi-wakka (finger ring) test the AUC derived from CC showed less variation (AUC: 0.877 0.906)
(stable) in the total cohort, males, and females, and was less affected
For the Yubi-wakka (finger-ring) test, we used binary logistic by gender compared to the other metrics, with acceptable discrimi-
regression to analyze the risk of developing sarcopenia. Setting “big- nation. In addition, CC had the best sensitivity and AUC for screening
ger” as the reference group, the test results are statistically associated for sarcopenia compared with SARC-F and SARC-Calf, according to
with the presence of sarcopenia (“just fits” OR: 4.1, 95% CI: the AWGS 2019 criteria.
1.57 10.98; “small” OR: 27.5, 95% CI: 10.14 74.55) for the total The second-best metric was SARC-Calf (AUC: 0.824 0.941), which
cohort. Sixty (28.7%) participants were in the “bigger” group, 76 showed a difference between men and women (AUC: 0.941 vs.
(36.3%) in the “just fits” group, and 73 (34.9%) in the “smaller” group 0.824). The Yubi-wakka (finger-ring) test results were analyzed using
(Table 3). binary logistic regression with the “bigger” group as the reference
Among men, 15 (23.47%) were in the “bigger” group, 27 (42.18%) group, and the results showed that the “smaller” and “just fits”
in the “just fits” group, and 22 in the “smaller” group (34.37%). These groups were associated with sarcopenia. However, the “just fits”
assessments are statistically associated with the presence of sarcope- group of men was not significantly associated with sarcopenia.
nia (“just fits” OR: 2.7, 95% CI: 0.69 10.89 and “small” OR 10.6, 95% The results of our study are the same as those of Kim and Won33
CI: 2.69 42.24). Among women, 45 (31.03%) were in the “bigger” and Mo et al.34 both showing that CC prediction (AUC: 0.64, 0.79) out-
group, 49 (33.79%) in the “just fits” group, and 51 in the “smaller” performed SARC-Calf (AUC: 0.62, 0.70) and SARC-F (AUC: 0.51, 0.56).
group (35.17%). These assessments are also statistically associated Participants in a study by Lin et al.35 were peritoneal dialysis patients
with the presence of sarcopenia (“just fits” OR: 5.0, 95% CI: (mean age = 57.5 § 14.1 years), and also had CC values (AUC: 0.813)
1.33 19.15 and “small” OR 45.5, 95% CI: 11.93 173.4) (Table 3). better than SARC-Calf (AUC: 0.739) and SARC-F (AUC: 0.587). The
above studies and the results of the present study all showed that CC
has a good ability to predict sarcopenia, whether it is in older adults
in the community or middle-aged people on peritoneal dialysis.
Table 2
Lin et al.36 used the Ishii test, CC, SARC-F, and SARC-Calf for the
Sensitivity and specificity analyses, and ROC models for SARC-F, SARC-Calf and Calf cir-
cumference validation against the AWGS 2019 criteria (N=209).
assessment of sarcopenia in older adults in nursing homes. The
results showed that the Ishii test (AUC: 0.86) performed better than
Sensitivity Specificity AUC 95% CI CC (AUC: 0.67). In contrast to our study, the Ishii test23 covering age,
SARC-F ( 4) CC, and grip strength may be better at predicting sarcopenia in nurs-
Total (84/209) 54.1% 70.2% 0.687 0.614 0.760 ing home residents than using CC alone, because the health and func-
Men (13/64) 32.9% 95.2% 0.775 0.695 0.855 tional status of such patients are different from those of older adults
Women (71/145) 65.5% 61.1% 0.704 0.619 0.789
in the community.
SARC-Calf ( 11)
Total (102/209) 76.5% 73.4% 0.832 0.778 0.887 The AUC of SARC-F in our study was 0.687 0.775. The metric’s
Men (22/64) 69.9% 96.7% 0.941 0.903 0.978 sensitivity was low for the total population, males, and females.
Women (80/145) 83.6% 65.6% 0.824 0.756 0.891 These results are similar to those of previous studies, which also used
Calf circumference AWGS diagnostic criteria for sarcopenia. Woo et al.25 reported a sen-
Men (30/64) 86.7% 82.4% 0.906 0.827 0.986
Women (87/145) 85.5% 63.3% 0.877 0.819 0.935
sitivity of 4.8 9.4%; Kim et al.37 reported 24%, and Parra-Rodríguez et
al.38 reported 31.5% (all three studies used community-dwelling
Abbreviations: SARC-F: strength, assistance with walking, rising from a chair, climbing
stairs, and falls; SARC-Calf: SARC-F combined with calf circumference; ROC models:
older adults). A meta-analysis by Voelker et al.39 also showed low to
Receiver Operating Curve Model; AUC: The area under the ROC curve; 95% CI: 95% Con- moderate sensitivity (28.9% 55.3%) and moderate to high specificity
fidence Interval. (68.9% 88.9%), suggesting that this test should not be a priority for
Y.-H. Lin et al. / Geriatric Nursing 49 (2023) 157 163 161
Fig 2. The ROC curves of calf circumference against the AWGS criteria in men (A) and women (B).
use in sarcopenia screening. With respect to analysis by gender, we on Sarcopenia in Older People (EWGSOP2) diagnostic criteria. The
found a lower sensitivity and higher specificity for males, similar to demonstrated capacity of CC to predict sarcopenia (AUC: 0.82) agree
the previous results by Woo et al.25 This may be due to the self- with these findings despite the differences in study participants and
reported questionnaire, where men may tend to overestimate their diagnostic criteria.
physical performance, while women may tend to underestimate it.40 We suggest that the original cut-off values for the CC method are
The AUC of SARC-Calf was 0.824 0.941, which agrees with applicable since the original Japanese study population20 and our
previous studies where adding CC improved overall measurement Taiwanese study population had similar racial characteristics. How-
accuracy, sensitivity, and specificity.41 Similar results were ever, results from the Korean Frailty and Aging Cohort Study (KFACS)
obtained in the past when AWGS was used as the standard for by Kim et al.44 indicated optimal cut-off values of CC for low muscle
diagnosing sarcopenia. For example, Yang et al.41 found a sensi- mass of 35 cm (AUC: 0.81) for males and 33 cm (AUC: 0.72) for
tivity of 60.7% and a specificity of 94.7%; Urzi et al.42 found a sen- females. Although Kim et al.’s study used the same diagnostic criteria
sitivity of 77.4% and a specificity of 89.8%. However, as with for sarcopenia, the optimal cut-off point for men was different from
SARC-F, sensitivity in men was lower than in women (69.9% vs. ours. Cut-off values may need to be further varied to determine the
83.6%), similar to the results from Yang et al.41 In contrast to our most suitable thresholds for different situations. In future studies, the
findings, Ishimoto et al.43 suggested that reducing the SARC-Calf research population should be expanded to include people from dif-
cut-off score from 11 to 7 could improve sensitivity (76.3% vs. ferent countries and clinical settings, e.g., long-term care institutions
94.7%) and specificity (100% vs. 92.3%). This reduced cut-off may and hospitalized older adults, to confirm whether the cut-off value
be more useful in screening sarcopenia. needs to be adjusted. Alternatively, the Youden’s index46 could be
According to AWGS 2019 diagnostic criteria and the original study used to find the best cut-off values in different situations.
by Kawakami et al.20 the cut-off values recommended for the CC test The CC can reflect the muscle mass of lower extremities. The
are 34 cm in males and 33 cm in females. Using these cut-off val- actual finger ring size used in the Yubi-wakka (finger-ring) test (on
ues, we found an AUC of 0.877 0.906 for both genders, suggesting average, 33 cm for males and 31 cm for females) is similar to a rough
excellent detection capacity.31 Kim et al.44 proposed CC as a substi- CC measurement.21 Our results showed that the proportion of “just
tute for the DXA muscle mass measure that can reflect lower extrem- fits” and “smaller” outcomes in the Yubi-wakka (finger-ring) test was
ity muscle mass. Our results are similar to those of the original study about 53% (79/149) in older adults with sarcopenia, consistent with
for both genders (AUC: 0.94 in men, 0.84 in women),20 showing that the study by Nishikawa et al.47 which showed that the proportions of
these cut-off values apply to both groups of participants. A study by sarcopenia in patients with bigger, just fits, and smaller outcomes
Borges et al.45 used CC to predict sarcopenia in hospitalized older were 3.5% (5/142), 18.2% (6/33), and 33.3% (9/27), respectively.
adults with hip fractures in Spain using the European Working Group Although their study participants and diagnostic criteria of
Table 3
Binary logistic regression analysis: association between sarcopenia and the “Yubi-wakka” test (N=209).
Yubi-wakka
Bigger 6/60 1.00 Reference 3/15 1.00 Reference 3/45 1.00 Reference
Just fits 24/76 4.1 1.57 10.98 .004** 11/27 2.7 0.69 10.89 .150 13/49 5.0 1.33 19.15 .017**
Smaller 55/73 27.5 10.14 74.55 <.001*** 16/22 10.6 2.69 42.24 < .001*** 39/51 45.5 11.93 173.4 <.001***
Abbreviations: 95% CI: 95% Confidence Interval; OR, odds ratio.
* p < .05.
** p < .01.
*** p < .001.
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