Fnut 09 803924
Fnut 09 803924
Fnut 09 803924
Background: The prevalence of sarcopenia is high in older people with type 2 diabetes
mellitus (T2DM) and is now considered a critical problem in the healthcare sector.
However, the preferred screening tool for identifying sarcopenia remains unknown. Thus,
the aim of this study was to ensure that the diagnostic values of the SARC-F (strength,
assisting with walking, rising from a chair, climbing stairs, and falling) and SARC-CalF
(SARC and calf circumference) scales were compared with five reference diagnostic
criteria for sarcopenia.
Methods: This was a cross-sectional study. Patients diagnosed with diabetes were
Edited by: treated at the First Affiliated Hospital of Wenzhou Medical University. Appendicular
Srikanth Bellary,
Aston University, United Kingdom
skeletal muscle mass, muscle strength, and physical performance were assessed using
Reviewed by:
dual-energy X-ray absorptiometry, handgrip strength, and gait speed assessment. Five
Dan Waitzberg, diagnostic criteria for sarcopenia (Asian Working Group for Sarcopenia, International
University of São Paulo, Brazil
Working Group on Sarcopenia, Foundation for the National Institutes of Health,
Masahide Hamaguchi,
Kyoto Prefectural University Sarcopenia Project, Society on Sarcopenia Cachexia and Wasting Disorders, and
of Medicine, Japan European Working Group on Sarcopenia in Older People criteria) were utilized.
*Correspondence: Sensitivity and specificity analyses were performed on the SARC-CalF and SARC-
Hong Zhu
[email protected]
F scales. The diagnostic precision of both instruments was determined using the
receiver-operating characteristic (ROC) curves and area under the ROC curves (AUC).
Specialty section:
This article was submitted to Results: This study included 689 subjects (459 men and 230 women) with a mean
Clinical Nutrition, age of 58.1 ± 13.2 years. In accordance with the five reference diagnostic parameters,
a section of the journal
Frontiers in Nutrition
the prevalence of sarcopenia was between 4.5 and 19.2%. In addition, the range of
Received: 28 October 2021
sensitivity of SARC-F and SARC-CalF ranged from 61.4 to 67.4 and 82.6 to 91.8%,
Accepted: 28 February 2022 respectively. Concurrently, the specificity ranged from 63.1 to 67.3 and 51.5 to 61.2%,
Published: 31 March 2022
respectively. Overall, AUC values for SARC-CalF were higher than those for SARC-F,
Citation:
regardless of the diagnostic standard, sex, or age.
Xu Z, Zhang P, Chen Y, Jiang J,
Zhou Z and Zhu H (2022) Comparing Conclusion: The results of this study suggest that SARC-CalF significantly enhances
SARC-CalF With SARC-F
for Screening Sarcopenia in Adults the sensitivity and overall diagnosis of SARC-F. SARC-CalF appears to be an optimal
With Type 2 Diabetes Mellitus. screening tool for sarcopenia in adults with T2DM.
Front. Nutr. 9:803924.
doi: 10.3389/fnut.2022.803924 Keywords: type 2 diabetes mellitus, sarcopenia, SARC-F, SARC-CalF, specificity, sensitivity, diagnostic criteria
TABLE 1 | Five diagnostic criteria for sarcopenia and the cut-off applied.
EWGSOP1 SMI ≤ 7.26 kg/m2 for men HGS < 30 kg for men GS < 0.8 m/s for both gender
SMI ≤ 5.50 kg/m2 for women HGS < 20 kg for women
AWGS2019 SMI < 7 kg/m2 for men HGS < 28 kg for men GS < 1 m/s for both gender
SMI < 5.4 kg/m2 for women HGS < 18 kg for women
IWGS SMI ≤ 7.2 kg/m2 for men GS < 1 m/s for both gender
SMI ≤ 5.67 kg/m2 for women
SCWD SMI ≤ 6.81 kg/m2 for men GS < 1 m/s for both gender
SMI ≤ 5.18 kg/m2 for women
FNIH ASM/BMI < 0.789 for men HGS < 26 kg for men
ASM/BMI < 0.512 for women HGS < 16 kg for women
SMI, skeletal muscle mass index; ASM, appendicular skeletal muscle mass; BMI, body mass index; HGS, handgrip strength; GS, gait speed.
PPV, positive predictive value; NPV, negative predictive value; +LR, positive likelihood ratio; −LR, negative likelihood ratio; AUC, area under the ROC curves. Values within parentheses represent the 95%
TABLE 2 | Characteristics of the study population.
p-Valuea
<0.001
<0.001
<0.001
<0.001
0.052
Variable Overall (n = 689) Men (n = 459) Women (n = 230) p-Valuea
Age (years)* 58.1 ± 13.2 56.4 ± 13.6 61.7 ± 11.7 <0.001
Diabetes duration 10.0 (3.0, 15.0) 9.0 (2.0, 15.0) 10.0 (5.0, 15.3) 0.028
(years)‡
HbA1c (%)* 9.6 ± 2.4 9.7 ± 2.4 9.3 ± 2.3 0.040
FPG (mmol/L)* 8.9 ± 3.0 8.8 ± 2.8 9.1 ± 3.2 0.206
0.67 (0.63–0.71)
0.79 (0.76–0.82)
0.67 (0.63–0.70)
0.81 (0.78–0.84)
0.65 (0.62–0.69)
0.78 (0.74–0.81)
0.66 (0.62–0.69)
0.78 (0.75–0.81)
0.65 (0.62–0.69)
0.74 (0.71–0.77)
2hPG (mmol/L)* 19.8 ± 4.7 19.5 ± 4.6 20.4 ± 4.9 0.023
AUC
HOMA-IR‡ 2.7 (1.7, 4.6) 2.5 (1.5, 3.9) 3.4 (1.9, 5.2) <0.001
ALT (U/L)‡ 21.0 (14.0, 32.0) 23.0 (15.0, 35.0) 17.0 (13.0, 25.0) <0.001
AST (U/L)‡ 21.0 (17.0, 29.0) 22.0 (17.0, 31.0) 20.0 (17.0, 26.0) 0.007
eGFR* 95.2 ± 28.3 96.4 ± 30.6 92.8 ± 22.8 0.112
BMI (kg/m2 )* 23.6 ± 3.4 23.7 ± 3.4 23.2 ± 3.3 0.076
WC (cm)* 90.1 ± 9.4 90.5 ± 9.4 89.3 ± 9.4 0.133
CC (cm)* 33.7 ± 3.6 34.3 ± 3.6 32.5 ± 3.2 <0.001
0.6 (0.5–0.7)
0.3 (0.2–0.4)
0.6 (0.4–0.7)
0.2 (0.1–0.3)
0.6 (0.4–0.8)
0.2 (0.1–0.4)
0.5 (0.3–0.8)
0.2 (0.1–0.4)
0.6 (0.3–0.9)
0.2 (0.1–0.6)
HGS (kg)* 29.0 ± 10.5 33.6 ± 9.3 19.8 ± 5.8 <0.001
−LR
GS (m/s)* 1.0 ± 0.2 1.0 ± 0.2 0.9 ± 0.2 <0.001
ASM (kg)* 20.0 ± 4.4 22.1 ± 3.6 15.9 ± 2.6 <0.001
TABLE 3 | Sensitivity, specificity, PPV, NPV, +LR, and −LR analyses and ROC curves for SARC-F and SARC-CalF validation against varying sarcopenia criteria.
SMI (kg/m2 )* 7.3 ± 1.2 7.7 ± 1.1 6.4 ± 0.9 <0.001
ASM/BMI* 0.9 ± 0.2 0.9 ± 0.1 0.7 ± 0.1 <0.001
SARC-F‡ 0 (0, 1) 0 (0, 1) 1 (0, 1) <0.001
SARC-CalF‡ 3 (0, 10) 1 (0, 10) 10 (1, 11) <0.001
SARC-F 0.070
1.9 (1.6–2.2)
2.1 (1.9–2.4)
1.9 (1.6–2.3)
2.3 (2.0–2.5)
1.8 (1.5–2.2)
2.0 (1.8–2.2)
1.9 (1.5–2.3)
2.0 (1.7–2.2)
1.8 (1.3–2.3)
1.9 (1.6–2.1)
classification†
+LR
Non-sarcopenia 658 (95.5%) 443 (96.5%) 215 (93.5%)
Sarcopenia 31 (4.5%) 16 (3.5%) 15 (6.5%)
SARC-CalF <0.001
classification†
Non-sarcopenia 549 (79.7%) 386 (84.1%) 163 (70.9%)
Sarcopenia 140 (20.3%) 73 (15.9%) 67 (29.1%)
88.0 (85.5–90.2)
93.7 (91.0–95.6)
89.9 (87.5–91.9)
96.2 (93.8–97.6)
93.0 (90.8–94.6)
97.4 (95.2–98.6)
96.2 (94.5–97.5)
98.8 (97.1–99.5)
97.4 (95.9–98.4)
99.1 (97.5–99.7)
EWGSOP1 0.063
classification†
NPV %
27.4 (23.9–31.2)
31.1 (28.5–33.8)
19.8 (16.8–23.1)
21.0 (19.2–23.0)
12.5 (10.3–15.2)
13.0 (11.7–14.3)
7.6 (5.9–9.8)
8.1 (7.1–9.2)
Non-sarcopenia 607 (88.1%) 403 (87.8%) 204 (88.7%)
PPV %
a The p-value represents the difference between the SARC-F and SARC-CalF groups.
SCWD 0.092
classification†
Non-sarcopenia 640 (92.9%) 421 (91.7%) 219 (95.2%)
Sarcopenia 49 (7.1%) 38 (8.3%) 11 (4.8%)
FNIH 0.090
classification†
67.3 (63.3–71.2)
61.2 (57.0–65.3)
66.7 (62.7–70.6)
61.0 (56.8–65.0)
65.2 (61.3–69.0)
54.9 (50.8–58.9)
64.1 (60.2–67.8)
52.8 (48.9–56.7)
63.1 (59.3–66.8)
51.5 (47.6–55.4)
62.6 (53.1–71.5)
87.8 (80.4–93.2)
63.4 (52.0–73.8)
89.0 (80.2–94.9)
67.4 (52.5–80.1)
91.8 (80.4–97.7)
64.5 (45.4–80.8)
90.3 (74.2–98.0)
Sensitivity %
confidential intervals.
SCWD classification
FNIH classification
SARC-CalF
SARC-CalF
SARC-CalF
SARC-CalF
SARC-F
SARC-F
SARC-F
SARC-F
FIGURE 1 | The ROC curves of SARC-F and SARC-CalF were contrasted with various reference standards in the entire population studied: (A) sarcopenia
according to the EWGSOP1 criteria; (B) sarcopenia according to AWGS2019 criteria; (C) sarcopenia according to IWGS criteria; (D) sarcopenia according to SCWD
criteria; and (E) sarcopenia according to FNIH criteria.
China) by experienced radiologists. Before analysis, subjects when the subjects were in a sitting position with their soles
were required to wear only a hospital gown and all-metal touching the surfaces of the floor, with the assumption that the
accessories. Scanning was taken while lying down. The software widest circumference of the right calf was being used. Waist
provides estimates of appendicular skeletal muscle mass (ASM), circumference (WC) was measured midway between the top of
which is the sum of lean body mass in the upper and the hip bone and the lower rib when the subjects were in a
lower extremities (14). The ASM assessed and calculated standing position. The measurement of the CC and WC required
the skeletal muscle mass index (SMI) and ASM/body mass the use of anthropometric tape. CC and WC must be accurate to
index (BMI). The SMI was computed from the equation: the nearest 0.1 cm.
ASM (kg)
SMI (kg/m2 ) = 2 . After fasting overnight, blood samples were taken from
height (m )
2
the antecubital vein and centrifuged at 5000 rpm for
The muscle strength was assessed on the basis of handgrip
20 min. Before conducting the assay, the plasma was stored
strength (HGS) using a portable electronic dynamometer
in freezing tubes at −80◦ C. Biochemical indices include
with a precision of 0.1 kg (Brand: CAMRY, Model: TH-01,
glycated hemoglobin (HbA1c), fasting plasma glucose (FPG),
XIANGSHAN, Zhongshan, and Guangdong Province, China).
2-h postprandial glucose (2hPG), alanine aminotransferase
Subjects who performed the HGS test were seated with their arms
(ALT), and aspartate aminotransferase (AST). All items
at their sides and with their elbows flexed at 90◦ . They squeezed
were assessed in the Biochemistry Department of the First
the handle as hard as they could. Trained surveyors assessed the
Affiliated Hospital of Wenzhou Medical University. Insulin
subject’s dominant hand three times, with an interval of 1 min
resistance (IR) was assessed through the application of the
between each measurement. All measured values were recorded,
homeostasis model (HOMA-IR), which was computed as
and the maximum value was taken as the muscle strength. FPG(mmol/l)∗ FINS(mIU/l)
In this study, the gait speed (GS) test was measured as the follows: HOMA−IR = (15), and the
22.5
physical performance. The subjects were instructed to walk a estimated glomerular filtration rate (eGFR) was computed in
distance of 6 m in their normal gait. If necessary, canes and accordance with the CKD-EPI formula (16).
walkers were adopted. The GS measurement was performed twice
with an accuracy of 0.1 m, and the mean value was recorded.
Assessment of Sarcopenia Using
Different Diagnostic Criteria
Clinical Data The five diagnostic classifications are utilized for screening
General clinical data, such as demographic information, duration sarcopenia: (1) the European Working Group on Sarcopenia
of illness, medical history, and medication status, were collected. in Older People (EWGSOP) (17); (2) the AWGS (5);
All anthropometric measurements were performed in the (3) the International Working Group on Sarcopenia
morning without eating before the assessments. Trained nurses (IWGS) (18); (4) the Society on Sarcopenia Cachexia and
measured weight (kg) and height (m) at 0.1 kg and 0.1 cm, Wasting Disorders (SCWD) (19); and (5) the Foundation
respectively. BMI (kg/m2 ) was computed as the body weight for the National Institutes of Health (FNHI) Sarcopenia
divided by the square of the height. The CC was assessed Project (20).
TABLE 4 | Sensitivity, specificity, PPV, NPV, +LR, and −LR analyses and ROC curves for SARC-F and SARC-CalF validation against different sarcopenia criteria in men.
EWGSOP1 classification
SARC-F 55.7 (45.2–65.8) 74.9 (70.1–79.2) 37.2 (31.6–43.3) 86.3 (83.3–88.8) 2.2 (1.7–2.8) 0.6 (0.5–0.7) 0.67 (0.62–0.71) <0.001
SARC-CalF 83.5 (74.6–90.3) 64.6 (59.5–69.6) 38.8 (34.9–42.7) 93.6 (90.3–95.8) 2.4 (2.0–2.8) 0.3 (0.2–0.4) 0.80 (0.76–0.84)
AWGS2019 classification
SARC-F 57.3 (45.9–68.2) 74.0 (69.3–78.4) 32.4 (27.1–38.2) 88.9 (86.0–91.2) 2.2 (1.7–2.8) 0.6 (0.4–0.7) 0.67 (0.63–0.71) <0.001
SARC-CalF 86.6 (77.3–93.1) 66.8 (61.8–71.6) 36.2 (32.5–40.2) 95.8 (92.9–97.6) 2.6 (2.2–3.1) 0.2 (0.1–0.3) 0.83 (0.79–0.86)
IWGS classification
SARC-F 62.5 (48.5–75.1) 72.7 (68.1–77.0) 24.1 (19.7–29.2) 93.3 (90.8–95.2) 2.3 (1.8–3.0) 0.5 (0.4–0.7) 0.68 (0.64–0.72) <0.001
SARC-CalF 91.1 (80.4–97.0) 57.3 (52.3–62.2) 22.9 (20.5–25.4) 97.9 (95.2–99.1) 2.1 (1.9–2.5) 0.2 (0.1–0.4) 0.80 (0.77–0.84)
SCWD classification
SARC-F 63.2 (46.0–78.2) 71.3 (66.7–75.5) 16.6 (13.0–20.9) 95.5 (93.4–97.0) 2.2 (1.7–2.9) 0.5 (0.3–0.8) 0.67 (0.62–0.71) <0.001
SARC-CalF 86.8 (71.9–95.6) 61.3 (56.4–66.0) 16.8 (14.6–19.4) 98.1 (95.8–99.2) 2.2 (1.9–2.7) 0.2 (0.1–0.5) 0.80 (0.76–0.84)
FNIH classification
SARC-F 64.0 (42.5–82.0) 70.3 (65.7–74.5) 11.0 (8.2–14.7) 97.1 (95.2–98.3) 2.2 (1.6–3.0) 0.5 (0.3–0.9) 0.68 (0.64–0.72) 0.076
SARC-CalF 92.0 (74.0–99.0) 57.1 (52.3–61.9) 11.0 (9.5–12.7) 99.2 (97.0–99.8) 2.2 (1.8–2.5) 0.2 (0.1–0.5) 0.77 (0.73–0.81)
PPV, positive predictive value; NPV, negative predictive value; +LR, positive likelihood ratio; −LR, negative likelihood ratio; AUC, area under the ROC curves. Values within
parentheses represent the 95% confidential intervals.
a The p-value represents the difference between the SARC-F and SARC-CalF groups.
FIGURE 2 | The ROC curves of SARC-F and SARC-CalF compared with various reference standards in men: (A) sarcopenia according to the EWGSOP1 criteria;
(B) sarcopenia according to AWGS2019 criteria; (C) sarcopenia according to IWGS criteria; (D) sarcopenia according to SCWD criteria; and (E) sarcopenia
according to FNIH criteria.
Sarcopenia was defined according to the EWGSOP1 and diagnostic precision and calculate the area under the ROC curves
AWGS2019 criteria as low muscle mass, in addition to low (AUC) at a 95% confidence interval (CI). Overall, AUCs <0.5,
muscle strength or low physical performance. According to the 0.5–0.7, 0.7–0.9, and >0.9 demonstrate that a tool has no, low,
IWGS and SCWD criteria, sarcopenia is defined as low muscle moderate, and high diagnostic values (21). The AUC values for
mass and poor physical performance. According to the FNHI each ROC curve were compared using the DeLong method (22).
recommendation, sarcopenia is defined as a low muscle mass The data were also stratified by age and sex to investigate the
associated with low muscle strength. Various diagnostic criteria capacity and application of the two screening tools.
recommended different cut-off values and were inconsistent for
both sexes. The comprehensive criteria used in this study are
listed in Table 1. RESULTS
TABLE 5 | Analysis of the curves of sensitivity, specificity, PPV, VPN, +LR, and −LR and ROC for the validation of SARC-F and SARC-CalF against various criteria of
sarcopenia in women.
EWGSOP1 classification
SARC-F 51.4 (34.0–68.6) 83.1 (77.1–88.1) 35.3 (25.9–46.0) 90.5 (87.1–93.1) 3.0 (1.9–4.8) 0.6 (0.4–0.8) 0.72 (0.65–0.77) 0.025
SARC-CalF 68.6 (50.7–83.1) 78.0 (71.5–83.6) 35.8 (28.3–44.1) 93.3 (89.4–95.8) 3.1 (2.2–4.4) 0.4 (0.2–0.7) 0.80 (0.74–0.85)
AWGS2019 classification
SARC-F 48.5 (30.8–66.5) 82.2 (76.2–87.3) 31.4 (22.4–42.1) 90.5 (87.2–93.0) 2.7 (1.7–4.3) 0.6 (0.4–0.9) 0.70 (0.63–0.75) 0.005
SARC-CalF 69.7 (51.3–84.4) 77.7 (71.2–83.3) 34.3 (27.0–42.4) 93.9 (90.1–96.3) 3.1 (2.2–4.4) 0.4 (0.2–0.7) 0.80 (0.74–0.85)
IWGS classification
SARC-F 38.5 (20.2–59.4) 79.9 (73.7–85.2) 19.6 (12.3–29.9) 91.1 (88.2–93.3) 1.9 (1.1–3.3) 0.8 (0.6–1.1) 0.61 (0.54–0.67) 0.006
SARC-CalF 88.5 (69.8–97.6) 48.0 (41.0–55.1) 17.8 (15.2–20.8) 97.0 (91.8–99.0) 1.7 (1.4–2.1) 0.2 (0.1–0.7) 0.73 (0.67–0.79)
SCWD classification
SARC-F 54.6 (23.4–83.3) 79.5 (73.5–84.6) 11.8 (6.8–19.5) 97.2 (94.8–98.5) 2.7 (1.5–4.8) 0.6 (0.3–1.1) 0.70 (0.64–0.76) 0.248
SARC-CalF 72.7 (39.0–94.0) 73.1 (66.7–78.8) 11.9 (8.2–17.1) 98.2 (95.3–99.3) 2.7 (1.8–4.1) 0.4 (0.1–1.0) 0.78 (0.72–0.83)
FNIH classification
SARC-F 50.0 (11.8–88.2) 78.6 (72.6–83.8) 5.9 (2.6–12.6) 98.3 (96.3–99.2) 2.3 (1.0–5.4) 0.6 (0.3–1.4) 0.62 (0.56–0.69) 0.227
SARC-CalF 66.7 (22.3–95.7) 71.9 (65.5–77.7) 6.0 (3.4–10.4) 98.8 (96.3–99.6) 2.4 (1.3–4.3) 0.5 (0.1–1.4) 0.70 (0.64–0.76)
PPV, positive predictive value; NPV, negative predictive value; +LR, positive likelihood ratio; −LR, negative likelihood ratio; AUC, area under the ROC curves. Values within
parentheses represent the 95% confidential intervals.
a The p-value represents the difference between the SARC-F and SARC-CalF groups.
FIGURE 3 | The ROC curves of SARC-F and SARC-CalF compared with various reference standards in women: (A) sarcopenia according to the EWGSOP1 criteria;
(B) sarcopenia according to AWGS2019 criteria; (C) sarcopenia according to IWGS criteria; (D) sarcopenia according to SCWD criteria; and (E) sarcopenia
according to FNIH criteria.
was 4.5 and 20.3%, respectively. According to the recommended In contrast, the least AUC against the IWGS and FNIH
cut-off values for various diagnostic criteria, the prevalence of criteria was recorded in SARC-F (0.65), and it likewise had a
sarcopenia was 19.2, 16.7, 11.9, 7.1, and 4.5%. The prevalence correspondingly small AUC for EWGSOP (0.67), AWGS2019
of sarcopenia varied between 5.4 and 21.1% in men and 2.6 (0.67), and SCWD (0.66).
and 15.2% in women. Irrespective of the reference benchmarks
applied, sarcopenia was more common in men than in women; Comparison of SARC-F and SARC-CalF
however, the differences were not significant. in Each Sex
Table 4 presents the results of sensitivity/specificity analyses and
Comparison of SARC-F and SARC-CalF AUCs of SARC-F and SARC-CalF in humans using various
in the Whole Study Population diagnostic criteria as reference standards. In men, SARC-CalF
Table 3 presents the results of sensitivity/specificity analyses, as displayed more suitable sensitivity as a reference standard,
well as the AUC of SARC-F and SARC-CalF in the course of regardless of diagnostic criteria; however, in contrast with SARC-
applying various diagnostic criteria as the reference benchmark. F, it displays a lower specificity. For instance, using EWGSOP1
The sensitivity of the two tools varied in the following ranges: as a reference standard, the sensitivities of SARC-F and SARC-
SARC-F, 61.4–67.4%; and SARC-ClaF, 82.6–91.8%. The values CalF were 55.7 and 83.5%, and the specificities were 74.9
of the specificity ranges were as follows: SARC-F, 63.1–67.3%; and 64.6%, respectively. In Figure 2, the ROC curves for
and SARC-ClaF, 51.5–61.2%. The PPV outcomes ranged from SARC-F and SARC-CalF against various reference standards in
7.6% (for SARC-F against FNIH) to 33.5% (for SARC-CalF men are depicted. Through the application of the EWGSOP1
against EWGSOP1), while a deviation is recorded in NPV as criteria, the respective AUC values for SARC-F and SARC-CalF
it varies from 88.0% (for SARC-F against EWGSOP1) to 99.1% were 0.67 and 0.80. Therefore, the difference was significant
(for SARC-CalF against FNIH). Irrespective of the type of (p < 0.001). In this study, the corresponding outcomes were
diagnostic criteria utilized as the reference standard, compared obtained using AWGS2019, IWGS, and SCWD. Assuming that
to the SARC-F, the SARC-CalF had more suitable sensitivity and the FNIH criteria were applied, there was no significant difference
lower specificity. (p = 0.076).
As shown in Figure 1, the ROC curves of the two Table 5 presents the results of sensitivity/specificity analyses,
screening tools against various standards in the entire study as well as the AUCs of SARC-F and SARC-CalF in women
population are plotted. The ranges of AUCs of SARC-F and with diverse diagnostic criteria serving as a reference benchmark.
SARC-CalF are 0.65–0.67 and 0.74–0.81, respectively. Regarding Regardless of the adopted reference standard utilized for women,
the AUCs, unless the FNIH criteria were implemented, the SARC-CalF equally demonstrated more suitable sensitivity and
variation between SARC-F and SARC-CalF was statistically identical specificity in contrast to SARC-F. For instance, when
significant (p < 0.001). When comparing the two screening using EWGSOP1 as the reference standard, the sensitivities
tools, the SARC-CalF had the most significant AUC but only of SARC-F and SARC-CalF were 51.4 and 68.6%, and the
against the AWGS2019 criteria (0.81). These outcomes indicate specificities were 83.1 and 78.0%, respectively. The ROC curves
that a nearly high level of diagnostic value was recorded. for SARC-F and SARC-CalF against various reference standards
TABLE 6 | Sensitivity, specificity, PPV, VPN, +LR, and −LR tests and ROC curves for SARC-F and SARC-CalF validation against various sarcopenia criteria in the older
group.
EWGSOP1 classification
SARC-F 41.1 (30.8–52.0) 80.7 (75.0–85.6) 45.1 (36.4–54.1) 78.0 (74.7–81.0) 2.1 (1.5–3.1) 0.7 (0.6–0.9) 0.63 (0.57–0.68) <0.001
SARC-CalF 84.4 (75.3–91.2) 54.9 (48.3–61.4) 42.0 (38.0–46.1) 90.1 (84.8–93.8) 1.9 (1.6–2.2) 0.3 (0.2–0.5) 0.75 (0.70–0.80)
AWGS2019 classification
SARC-F 42.5 (31.0–54.6) 79.6 (74.1–84.4) 37.8 (29.7–46.6) 82.6 (79.4–85.4) 2.1 (1.4–3.0) 0.7 (0.6–0.9) 0.64 (0.58–0.69) <0.001
SARC-CalF 90.4 (81.2–96.1) 54.0 (47.6–60.3) 36.5 (33.0–40.1) 95.1 (90.4–97.5) 2.0 (1.7–2.3) 0.2 (0.1–0.4) 0.78 (0.74–0.83)
IWGS classification
SARC-F 66.0 (51.7–78.5) 51.9 (45.7–57.9) 21.2 (17.6–25.3) 88.6 (84.0–92.0) 1.4 (1.1–1.7) 0.7 (0.4–1.0) 0.60 (0.54–0.65) <0.001
SARC-CalF 88.7 (77.0–95.7) 50.4 (44.2–56.5) 26.0 (23.1–29.0) 95.8 (91.4–98.0) 1.8 (1.5–2.1) 0.2 (0.1–0.5) 0.73 (0.68–0.78)
SCWD classification
SARC-F 69.0 (49.2–84.7) 50.7 (44.8–56.5) 12.1 (9.5–15.3) 94.3 (90.5–96.6) 1.4 (1.1–1.8) 0.6 (0.4–1.1) 0.59 (0.53–0.64) <0.001
SARC-CalF 93.1 (77.2–99.2) 47.6 (41.8–53.5) 14.9 (13.1–16.9) 98.6 (94.8–99.6) 1.8 (1.5–2.1) 0.2 (0.1–0.6) 0.73 (0.68–0.78)
FNIH classification
SARC-F 68.0 (46.5–85.1) 50.3 (44.5–56.2) 10.3 (7.9–13.3) 94.9 (91.3–97.1) 1.4 (1.0–1.8) 0.6 (0.4–1.1) 0.60 (0.54–0.65) 0.195
SARC-CalF 92.0 (74.0–99.0) 42.0 (36.3–47.8) 11.7 (10.3–13.4) 98.4 (94.3–99.6) 1.6 (1.4–1.8) 0.2 (0.1–0.7) 0.67 (0.61–0.72)
PPV, positive predictive value; NPV, negative predictive value; +LR, positive likelihood ratio; −LR, negative likelihood ratio; AUC, area under the ROC curves. Values within
parentheses represent the 95% confidential intervals. a The p-value represents the difference between the SARC-F and SARC-CalF groups.
FIGURE 4 | The ROC curves of SARC-F and SARC-CalF compared with various reference norms in the older group: (A) sarcopenia according to the EWGSOP1
criteria; (B) sarcopenia according to AWGS2019 criteria; (C) sarcopenia according to IWGS criteria; (D) sarcopenia according to SCWD criteria; and (E) sarcopenia
according to FNIH criteria.
in women are shown in Figure 3. Using the EWGSOP1 criteria, demonstrated that the AUC of the two screening tools was higher
the AUCs for SARC-F and SARC-CalF were 0.72 and 0.80, in the younger subjects than in the older subjects. Furthermore,
respectively. There was a significant difference between the it was observed that the increase in age is directly proportional
groups (p = 0.025). With the assistance of AWGS2019 and to the increase in sensitivity to SARC-CalF. In contrast, a
IWGS, similar results were obtained. The AUC of SARC-CalF contradictory trend was demonstrated in the specificity of SARC-
is moderate when applied to different sensitivities to various CalF.
reference benchmarks when applied for different sexes.
DISCUSSION
Comparison of SARC-F and SARC-CalF
in Each Age Group This study showed that SARC-CalF was significantly more
Table 6 presents the screening potential of SARC-F alongside suitable than SARC-F in sarcopenia screening for patients
SARC-CalF in subjects aged ≥60 years during the application with T2DM in terms of sensitivity and general diagnostic
of various diagnostic criteria as reference standards. accuracy using varying criteria as a gold benchmark. Since
Sensitivity/specificity analyses showed related results in the sarcopenia is associated with serious consequences on the
older group, in contrast to the entire study population. The health of older subjects, early recommendation of preventive
sensitivity of the two instruments varied in the following areas: strategies is highly necessary. Thus, from a clinical perspective,
SARC-F, 41.1–69.0%; and SARC-CalF, 84.4–93.1%. The ranges of it is essential to provide an early diagnosis using simple and
specificity were as follows: SARC-F, 50.3–80.7%; and SARC-CalF, effective sarcopenia screening tools, preferably, a screening tool
42.0–54.9%. As shown in Figure 4, during the process of applying exhibiting high sensitivity while simultaneously maintaining high
the EWGSOP1, AWGS2019, IWGS, and SCWD, the variation in specificity (23).
AUC between SARC-F and SARC-CalF was generally significant. Based on the general consensus about sarcopenia, for
Table 7 presents the screening potentials of SARC-F and diagnosis confirmation, it has been demonstrated that low muscle
SARC-CalF in subjects aged <60 years with varying diagnostic mass and function are essential. SARC-F is the first screening
criteria as a reference standard. In the younger group, the tool for sarcopenia and has been widely applied in the field of
sensitivity of the two instruments varied in the following areas: sarcopenia. Thus far, the validation of the research has been
SARC-F, 33.3–65.0%; and SARC-Calf, 83.3–90.0%. The ranges of implemented in China (8, 12, 24), America (25), Japan (26),
specificity were as follows: SARC-F, 75.4–92.2%; and SARC-CalF, Turkey (10), and Brazil (27, 28), to mention a few. Nevertheless,
59.3–62.4%. As shown in Figure 5, there is a significant variation previous studies have revealed that it has high specificity and low
in AUC between SARC-F and SARC-CalF when the EWGSOP1, sensitivity. A novel study conducted by Parra-Rodríguez et al.
AWGS2019, and IWGS criteria were applied. revealed that in 487 men and women, the sensitivity to SARC-
In the category of older subjects, the AUC of the two F was 35.6% with a specificity of 82.2% (9). The outcome of this
instruments was from 0.59 to 0.78, while it was from 0.64 to study corresponds to the results of Woo et al., which revealed
0.82 in younger subjects. Therefore, a comparison of both groups that the sensitivity and specificity of SARC-F were 9.9 and 94.4%,
TABLE 7 | Sensitivity, specificity, PPV, NPV, +LR, and −LR assessments and ROC curves for SARC-F and SARC-CalF validation against various criteria of sarcopenia in
the group comprising of the younger group.
EWGSOP1 classification
SARC-F 57.1 (41.0–72.3) 77.2 (72.2–81.6) 24.5 (18.9–31.1) 93.3 (90.7–95.2) 2.5 (1.8–3.5) 0.6 (0.4–0.8) 0.69 (0.64–0.73) 0.005
SARC-CalF 83.3 (68.6–93.0) 61.7 (56.2–67.0) 22.0 (18.9–25.5) 96.6 (93.5–98.3) 2.2 (1.8–2.6) 0.3 (0.1–0.5) 0.80 (0.76–0.84)
AWGS2019 classification
SARC-F 54.8 (38.7–70.2) 76.9 (71.9–81.3) 23.5 (17.9–30.1) 92.9 (90.3–94.8) 2.4 (1.7–3.3) 0.6 (0.4–0.8) 0.67 (0.62–0.72) <0.001
SARC-CalF 88.1 (74.4–96.0) 62.4 (56.8–67.6) 23.3 (20.2–26.6) 97.6 (94.6–98.9) 2.3 (2.0–2.8) 0.2 (0.1–0.4) 0.82 (0.77–0.85)
IWGS classification
SARC-F 58.6 (38.9–76.5) 76.0 (71.0–80.4) 17.3 (12.8–23.1) 95.5 (93.2–97.1) 2.4 (1.7–3.5) 0.5 (0.4–0.8) 0.68 (0.63–0.73) 0.017
SARC-CalF 89.7 (72.6–97.8) 60.5 (55.1–65.8) 16.4 (14.0–19.0) 98.6 (95.9–99.5) 2.3 (1.9–2.7) 0.2 (0.1–0.5) 0.79 (0.75–0.83)
SCWD classification
SARC-F 65.0 (40.8–84.6) 75.4 (70.5–79.9) 13.3 (9.5–18.1) 97.4 (95.3–98.5) 2.7 (1.8–3.8) 0.5 (0.3–0.8) 0.72 (0.67–0.76) 0.090
SARC-CalF 90.0 (68.3–98.8) 59.3 (53.9–64.5) 11.3 (9.5–13.4) 99.0 (96.5–99.7) 2.2 (1.8–2.7) 0.2 (0.1–0.6) 0.80 (0.76–0.84)
FNIH classification
SARC-F 33.3 (4.3–77.7) 92.2 (89.0–94.8) 6.7 (2.1–19.0) 98.8 (97.9–99.3) 4.3 (1.3–14.0) 0.7 (0.4–1.3) 0.64 (0.59–0.69) 0.143
SARC-CalF 83.3 (35.9–99.6) 61.4 (56.1–66.4) 3.5 (2.4–5.0) 99.5 (97.4–99.9) 2.2 (1.5–3.2) 0.3 (0.1–1.6) 0.77 (0.72–0.81)
PPV, positive predictive value; NPV, negative predictive value; +LR, positive likelihood ratio; −LR, negative likelihood ratio; AUC, area under the ROC curves. Values within
parentheses represent the 95% confidential intervals.
a The p-value represents the difference between the SARC-F and SARC-CalF groups.
FIGURE 5 | The ROC curves of SARC-F and SARC-CalF compared with various reference standards in the category of younger subjects: (A) sarcopenia according
to the EWGSOP1 criteria; (B) sarcopenia according to AWGS2019 criteria; (C) sarcopenia according to IWGS criteria; (D) sarcopenia according to SCWD criteria;
and (E) sarcopenia according to FNIH criteria.
respectively (8). Thus, due to the low sensitivity of SARC-F, it has SARC-F, demonstrating moderate diagnostic accuracy; the CC
subsequently brought about limitations to its clinical application. per se was not significantly better than the SARC-CalF. In
From the findings of Kawakami et al., a positive correlation contrast, the SARC-CalF was slightly more sensitive than the
was found between CC and muscle mass (29). Furthermore, CC. This finding should be addressed in future studies with
the SARC-CalF, integrating CC and SARC-F, was developed larger sample sizes. Overall, the conclusions remain unchanged.
by Barbosa-Silva. This research, which involved 179 older These data are shown in Supplementary Table 2. Moreover,
people in communities in Brazil, found that the sensitivity a novel tool, known as the mini sarcopenia risk assessment
and specificity of SARC-CalF were 66.7 and 82.9%, respectively (MSRA) questionnaire, was developed by Rossi et al., with
(11). Following the application of the same standard, it was sensitivity and specificity of 80.4 and 60.4%, respectively. The
reported by Yang et al. that SARC-CalF with sensitivity and MSRA includes a comprehensive evaluation and nutritional
specificity in Chinese nursing home occupants was 58.9 and assessment (36). This scale was validated in the study by Ming-
84.5%, respectively (13). Therefore, it was proposed by the Yang et al. in various populations and subsequently surmised that
above researchers that SARC-CalF should be utilized as a MSRA-5 could act as a dependable and valid tool for screening
modified version for enhancing the sensitivity of SARC-F sarcopenia (13, 37). Through the application of age, as well as
(11). In this study, the sensitivity and specificity displayed by BMI, Kurita et al. enhanced SARC-F and named this modified
SARC-CalF were 82.6 and 61.2%, respectively, by applying the version SARC-F + EBM (38). In 2019, research conducted on 959
EWGSOP1 criteria. In contrast to past research, this study hospitalized Japanese patients showed that SARC-F + EBM had
showed relatively lower specificity, albeit a higher sensitivity, higher sensitivity than SARC-F, with a sensitivity of 77.8% and
possibly as a result of the varying clinical features (race, sex, a specificity of 69.6% (38). Thus, the validation and comparison
and age) of the subjects. In addition, all subjects in the study of these new screening tools in adults with T2DM should be
have diabetes. Applying various diagnostic criteria, the AUC evaluated in subsequent studies.
of SARC-F ranged from 0.65 to 0.67, and the AUC of SARC- Certain drawbacks of this study need to be addressed. First,
CalF ranged from 0.74 to 0.81. Thus, SARC-F displayed low this study focused initially only on hospitalized patients with
diagnostic precision, and SARC-CalF demonstrated moderate T2DM. Thus, this study outcome may not be appropriate for
diagnostic accuracy. In general, with regard to the screening older people residing in the community. Second, cognitive
for sarcopenia in adults with T2DM, SARC-CalF is more functions were not assessed because our subjects were relatively
effective than SARC-F. young. Notwithstanding, SARC-F was developed based on the
This study demonstrated that sex and age could affect elderly population. Third, the prognostic value of SARC-F and
the screening potential of the two screening tools. Overall, SARC-CalF for adverse outcomes should be considered in future
men tend to overestimate their physical abilities (30), while prospective studies as a cross-sectional study.
women could underestimate their physical abilities because of
their diverse perceptions. The results of this study showed
that SARC-F and SARC-CalF have significantly higher values CONCLUSION
in women than in men. Regarding sex, SARC-CalF in men
showed higher sensitivity and AUC compared with women. In summary, early detection and intervention of sarcopenia
This result in contrast to the conclusion of Mo et al. (31). are crucial. Regardless of the reference standard, sex, and age,
Moreover, age was one of the criteria. In general, the specificity SARC-CalF displayed more suitable sensitivity and diagnostic
and AUC of SARC-CalF decreased with age. In contrast, performance than SARC-F. Thus, SARC-CalF appears to be a
the trend displayed by the sensitivity of SARC-CalF showed more appropriate screening tool for sarcopenia in adults with
the opposite trend. This result corroborate the study by T2DM. Subsequent research is needed to validate the utility of
Mo et al. (31). SARC-CalF in various populations and frameworks.
Calf circumference tends to be profoundly impacted by obesity
and edema, which may mask sarcopenia (13, 32). Nevertheless, STANDARD BIOSECURITY AND
various optimal cut-off points exist for CC in various ethnic
groups. Kawakami et al. utilized 34 and 33 cm as cut-off points
INSTITUTIONAL SAFETY PROCEDURES
for CC in Japanese men and women, respectively, in estimating All institutional security procedures were followed and
low muscle mass (29). In a Turkish study, 33 cm was proposed biosecurity metrics were implemented. The hospital laboratory
as the threshold point for CC in men and women (33). In a utilized for this research has a biosafety level 2 (BSL-2) standard,
recent study conducted by Hwang et al. in Taiwan, sections were implying that all standards and protocols have been implemented
recorded at 33 and 32 cm to predict sarcopenia in men and in accordance with the guidelines of the Clinical and Laboratory
women, respectively. In our study, the median CC in men and Standards Institute (CLSI).
women was 34 and 33 cm, respectively. Thus, the cut-off values
of the screening recommended by the AWGS2019 consensus are
appropriate for subjects utilized in this study. DATA AVAILABILITY STATEMENT
Recent studies have reported that the CC per se was better than
the SARC-F and SARC-CalF (31, 34, 35). Our data demonstrated The raw data supporting the conclusions of this article will be
that although both the SARC-CalF and CC outperformed the made available by the authors, without undue reservation.
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J Am Med Dir Assoc. (2021) 22:746–50.e1. doi: 10.1016/j.jamda.2020.05.041 endorsed by the publisher.
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to identify sarcopenia according to European working group on sarcopenia the original author(s) and the copyright owner(s) are credited and that the original
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