Comparison of the performance of five screening methods for sarcopenia

Figures & data

Table 1 Five operational definitions of sarcopenia and the cutoff limits applied

Diagnosis definition	Muscle mass	Muscle strength	Physical performance
Cruz-Jentoft et al^Citation18 (EWGSOP)	Women: SMI≤5.50 kg/m^2	Women: handgrip strength<20 kg	SPPB≤8
	Men: SMI≤7.26 kg/m^2	Men: handgrip strength<30 kg
Fielding et al^Citation19 (IWGS)	Women: SMI≤5.67 kg/m^2	Not applicable	Gait speed<1.0 m/s
	Men: SMI≤7.23 kg/m^2
Morley et al^Citation20 (Society of Sarcopenia, Cachexia and Wasting Disorders)	Women: SMI≤5.18 kg/m^2	Not applicable	Gait speed<1.0 m/s
	Men: SMI≤6.81 kg/m^2
Chen et al^Citation21 (AWGS)	Women: SMI≤5.40 kg/m^2	Women: handgrip strength<18 kg	Gait speed<0.8 m/s
	Men: SMI≤7.00 kg/m^2	Men: handgrip strength<26 kg
Studenski et al^Citation22 (FNIH Sarcopenia Project)	Women: ALMBMI <0.512	Women: handgrip strength<16 kg	Not applicable
	Men: ALMBMI <0.789	Men: handgrip strength<26 kg

Abbreviations: ALM, appendicular skeletal lean mass; AWGS, Asian Working Group for Sarcopenia; BMI, body mass index; EWGSOP, European Working Group on Sarcopenia in Older People; IWGS, International Working Group on Sarcopenia; SMI, skeletal muscle mass index; SPPB, Short Physical Performance Battery.

Table 2 Description of five screening strategies for sarcopenia

Study team	Type of screening tools	Aim of the tool	Principle and variables of interest	Authors’ categorization in “at risk” or “not at risk” of sarcopenia
Cruz-Jentoft et al^Citation18	Two-stage algorithm	To enable rapid identification of individuals who should undergo a thorough examination (i.e., measurement of muscle mass using DEXA) for the diagnosis of sarcopenia	Assessment of gait speed: if gait speed is too slow (≤0.8 m/s), measure muscle mass. If gait speed is >0.8 m/s, proceed to an assessment of grip strength: if grip strength is low (<20 kg for female, <30 kg for men), measure muscle mass	Subjects presenting a low gait speed or a low gait speed plus a low grip strength are considered “at risk of sarcopenia”
Malmstrom et al^Citation23	SARC-F questionnaire	To rapidly identify individuals who require a diagnostic examination for sarcopenia	Five-domain symptom-based questionnaire: strength, ambulation (walking independence), rising from a chair, stair climbing and history of falls. The total score is 10 points (with each component scoring 2)	A score of ≥4 points is predictive of sarcopenia
Goodman et al^Citation24	Screening grid	To use predictors of low muscle mass to identify subjects requiring a diagnostic evaluation of low muscle mass (using DEXA)	Screening grid built using age and BMI and developed for both men and women, It provides, according to the age and the BMI of the subject, the probability (%) of low muscle mass	Individuals with a probability (given by the grid) above 70% in men and above 80% in women are considered as having low muscle mass (i.e., at risk of sarcopenia)
Ishii et al^Citation25	Score chart	To identify older adults at high risk of sarcopenia	Probability of sarcopenia estimated using a score chart composed of three variables: age, grip strength and calf circumference. Score in men: 0.62×(age−64)−3.09×(grip strength−50)−4.64×(calf circumference−42). Probability in men: 1/1[1+e^−(sum score/10−11.9)]. Score in women: 0.80×(age−64)−5.09×(grip strength−34)−3.28×(calf circumference−42). Probability in women: 1/1[1+e^−(sum score/10−12.5)]	Sum score above 105 in men and 120 in women determines people having a high probability of sarcopenia
Yu et al^Citation26	Anthropometric prediction equation	To determine a prediction equation of a low muscle mass	Anthropometric prediction equation based on four parameters: weight, BMI, age and sex. Appendicular skeletal muscle mass prediction equation: 10.05+0.35(weight)−0.62(BMI)−0.02(age)+5.10(if male)	Subjects presenting a score, derived from the prediction equation, below the 20th percentile value (computed for our cohort) were considered “at risk of sarcopenia”

Abbreviations: BMI, body mass index; DEXA, dual-energy X-ray absorptiometry; EWGSOP, European Working Group on Sarcopenia in Older People.

Figure 1 Description of the participant population analyzed.

Abbreviation: SarcoPhAge, Sarcopenia and Physical Impairment with Advancing Age.

Table 3 Summary of participant characteristics (n=306)

Characteristics	Men (n=124)	Women (n=182)
Age (years)	75.0±5.9	74.7±5.9
Anthropometric data
Weight (kg)	171.6±6.7	157.9±6.8
Height (cm)	82.0±14.3	65.7±13.5
BMI (kg/m^2)	27.8±4.3	26.3±4.9
Calf circumference (cm)	35.8±3.2	33.7±3.4
Waist circumference (cm)	98.6±12.6	87.0±12.7
Wrist circumference (cm)	17.9±1.2	15.8±1.1
Arm circumference (cm)	28.5±3.1	27.2±3.2
Level of education
Without qualification	3 (2.4)	2 (1.1)
Primary school	10 (8.1)	18 (9.9)
Secondary school	53 (42.8)	94 (51.7)
Postsecondary education	55 (44.3)	65 (35.7)
Doctorate	3 (2.4)	3 (1.6)
Number of concomitant diseases by subject	4.1±2.6	4.3±2.4
Number of drugs consumed by subject	5.9±3.2	6.8±3.8
MMSE (/30 points)	28.7±1.5	28.8±2.0
SMI (kg/m^2)	7.9±1.0	6.1±0.9
Muscle strength (kg)	37.6±8.7	19.6±6.2
SPPB (/12 points)	10.2±1.1	9.6±1.2
4 m gait speed (m/s)	1.2±0.3	1.0±0.3
Prevalence of sarcopenia using Cruz-Jentoft et al’s criteria	19 (15.3)	32 (17.6)
Prevalence of sarcopenia using Fieldling et al’s criteria	16 (12.9)	21 (11.5)
Prevalence of sarcopenia using Morley et al’s criteria	8 (6.4)	10 (5.5)
Prevalence of sarcopenia using Chen et al’s criteria	5 (4.0)	12 (6.6)
Prevalence of sarcopenia using Studenski et al’s criteria	7 (5.6)	15 (8.2)

Abbreviations: BMI, body mass index; MMSE, Mini-Mental State Examination; SMI, skeletal muscle mass index; SPPB, Short Physical Performance Battery.

Table 4 Concordance between the five diagnostic definitions of sarcopenia and between the five screening methods

Diagnostic definitions	Definition of Cruz-Jentoft et al	Definition of Fielding et al	Definition of Morley et al	Definition of Chen et al	Definition of Studenski et al
Definition of Cruz-Jentoft et al	1	0.71 (0.66–0.76)	0.44 (0.38–0.50)	0.45 (0.39–0.51)	0.22 (0.17–0.27)
Definition of Fielding et al		1	0.62 (0.57–0.67)	0.56 (0.50–0.62)	0.20 (0.15–0.24)
Definition of Morley et al			1	0.48 (0.42–0.57)	0.14 (0.10–0.18)
Definition of Chen et al				1	0.26 (0.21–0.31)
Definition of Studenski et al					1
Screening tools	Two-stage algorithm of the EWGSOP	SARC-F of Malmstrom et al	Screening grid of Goodman et al	Score chart of Ishii et al	Equation of Yu et al
Two-stage algorithm of the EWGSOP	1	0.46 (0.40–0.52)	0.05 (0.03–0.07)	0.43 (0.37–0.48)	0.17 (0.13–0.21)
SARC-F of Malmstrom et al		1	0.05 (0.03–0.07)	0.29 (0.24–0.34)	0.13 (0.09–0.17)
Screening grid of Goodman et al			1	0.18 (0.14–0.22)	0.63 (0.58–0.68)
Score chart of Ishii et al				1	0.31 (0.26–0.36)
Equation of Yu et al					1

Abbreviation: EWGSOP, European Working Group on Sarcopenia in Older People.

Table 5 Indicators of performance of five screening methods across five definitions of sarcopenia (n=306)

Screening method according to diagnosis definition	Sensitivity, proportion, % (95% CI)	Specificity, proportion, % (95% CI)	PPV, probabilit, % (95% CI)	NPV, probability, % (95% CI)
Definition of Cruz-Jentoft et al
Two-stage algorithm of the EWGSOP	33.3 (28.0–38.6)	91.0 (87.8–94.2)	42.5 (37.0–48.0)	87.2 (83.5–90.9)
SARC-F of Malmstrom et al	36.0 (30.6–41.4)	87.1 (83.3–90.9)	35.3 (29.9–40.7)	87.4 (83.7–91.1)
Screening grid of Goodman et al	47.5 (41.9–53.1)	89.4 (86.0–92.8)	50.9 (45.3–56.5)	88.0 (84.4–91.6)
Score chart of Ishii et al	84.3 (80.2–88.4)	80.9 (76.5–85.3)	46.7 (41.1–52.3)	96.3 (94.2–98.4)
Equation of Yu et al	51.0 (45.4–56.6)	86.7 (82.9–90.5)	43.3 (37.7–48.9)	89.8 (86.4–93.2)
Definition of Fielding et al
Two-stage algorithm of the EWGSOP	43.2 (37.6–48.8)	91.1 (87.9–94.3)	40.0 (34.5–45.5)	92.1 (89.1–95.1)
SARC-F of Malmstrom et al	43.2 (37.6–48.8)	86.6 (82.8–90.4)	30.8 (25.6–36.0)	91.7 (88.6–94.8)
Screening grid of Goodman et al	45.9 (40.3–51.5)	88.8 (85.3–92.3)	36.2 (30.8–41.6)	92.3 (89.3–95.3)
Score chart of Ishii et al	86.8 (83.0–90.6)	77.7 (73.0–82.4)	34.8 (29.5–40.1)	97.7 (96.0–99.4)
Equation of Yu et al	64.9 (59.6–70.2)	86.6 (82.8–90.4)	40.0 (34.5–45.5)	94.7 (92.2–97.2)
Definition of Morley et al
Two-stage algorithm of the EWGSOP	38.9 (33.4–44.4)	88.5 (84.9–92.1)	17.5 (13.2–21.8)	95.9 (93.7–98.1)
SARC-F of Malmstrom et al	55.6 (50.0–61.2)	85.4 (81.4–91.4)	19.2 (14.8–23.6)	96.8 (94.8–98.8)
Screening grid of Goodman et al	66.7 (61.4–72.0)	87.8 (84.1–91.5)	25.5 (20.6–30.4)	97.7 (96.0–99.4)
Score chart of Ishii et al	100.0 (100–100)	74.3 (69.4–79.2)	34.8 (29.5–40.1)	97.7 (96.0–99.4)
Equation of Yu et al	83.3 (79.1–87.5)	84.4 (80.3–88.5)	25.0 (20.1–29.9)	98.8 (97.6–100)
Definition of Chen et al
Two-stage algorithm of the EWGSOP	70.6 (65.5–75.7)	90.3 (87.0–93.6)	30.0 (24.9–35.1)	98.1 (96.6–99.6)
SARC-F of Malmstrom et al	52.9 (47.3–58.5)	85.1 (81.1–89.1)	17.3 (13.1–21.5)	96.8 (94.8–98.8)
Screening grid of Goodman et al	41.2 (35.7–46.7)	86.2 (82.3–90.1)	14.9 (10.9–18.9)	96.1 (93.9–98.3)
Score chart of Ishii et al	100.0 (100–100)	74.1 (69.2–79.0)	14.5 (10.6–18.4)	100.0 (100–100)
Equation of Yu et al	16.1 (12.0–20.2)	60.0 (54.5–65.5)	42.0 (38.9–45.1)	91.1 (87.9–94.3)
Definition of Studenski et al
Two-stage algorithm of the EWGSOP	50.0 (44.4–55.6)	89.8 (86.4–93.2)	27.5 (22.5–32.5)	95.9 (93.6–98.0)
SARC-F of Malmstrom et al	40.9 (35.4–46.4)	84.9 (80.9–88.9)	17.3 (13.1–21.5)	94.9 (92.4–97.4)
Screening grid of Goodman et al	5.88 (3.20–8.50)	83.5 (79.3–87.7)	4.26 (2.0–6.50)	87.6 (83.9–91.3)
Score chart of Ishii et al	90.9 (87.7–94.1)	74.9 (70.0–79.8)	21.7 (17.1–26.3)	99.1 (98.0–100)
Equation of Yu et al	36.4 (31.0–41.8)	81.7 (77.4–86.0)	13.3 (9.50–17.1)	94.3 (91.7–96.9)

Abbreviations: EWGSOP, European Working Group on Sarcopenia in Older People; NPV, negative predictive value; PPV, positive predictive value.

Table 6 Association between the five definitions of sarcopenia and five screening tools (n=306)

Screening method according to diagnosis definition	Coefficient±standard error	Adjusted OR (95% CI)a	p-valuea	AUC (95% CI)	p-value of AUC comparison			Cutoff limits proposed
					Versus SARC-F	Versus screening grid	Versus score chart	Distance 0.1	Youden’s index
Definition of Cruz-Jentoft et al
Two-stage algorithm of the EWGSOP	0.43±0.427	3.43 (1.48–7.95)	0.0039
SARC-F of Malmstrom et al	0.32±0.069	1.30 (1.10–1.54)	0.0016	0.710 (0.636–0.785)				2	2
Screening grid of Goodman et al	0.07±0.005	1.03 (1.02–1.04)	<0.0001	0.752 (0.684–0.821)	0.4500			34.4	16.8
Score chart of Ishii et al	0.03±0.005	1.04 (1.03–1.06)	<0.0001	0.856 (0.807–0.906)	0.0006	0.0073		113.5	112.3
Equation of Yu et al	−0.21±0.054	0.71 (0.61–0.84)	<0.0001	0.688 (0.612–0.764)	0.6800	0.1800	<0.0001	15.99	15.21
Definition of Fielding et al
Two-stage algorithm of the EWGSOP	2.11±0.489	8.25 (3.15–21.6)	<0.0001
SARC-F of Malmstrom et al	0.38±0.090	1.47 (1.23–1.75)	<0.0001	0.764 (0.688–0.840)				2	2
Screening grid of Goodman et al	0.03±0.006	1.04 (1.02–1.05)	<0.0001	0.767 (0.682–0.851)	0.9700			61.3	61.3
Score chart of Ishii et al	0.04±0.007	1.05 (1.03–1.06)	<0.0001	0.841 (0.788–0.894)	0.0710	0.1400		117.2	111.1
Equation of Yu et al	−0.48±0.100	0.62 (0.51–0.76)	<0.0001	0.693 (0.607–0.779)	0.2300	0.2100	0.0001	15.49	16.79
Definition of Morley et al
Two-stage algorithm of the EWGSOP	1.88±0.632	6.61 (1.90–22.9)	0.0028
SARC-F of Malmstrom et al	0.46±0.120	1.05 (1.03–2.01)	0.0001	0.743 (0.641–0.872)				3	4
Screening grid of Goodman et al	0.06±0.012	1.06 (1.03–1.09)	<0.0001	0.853 (0.746–0.960)	0.2600			70.7	70.7
Score chart of Ishii et al	0.05±0.107	1.04 (1.01–1.08)	<0.0001	0.874 (0.825–0.922)	0.0430	0.7300		121.6	117.8
Equation of Yu et al	−0.53±0.135	0.58 (0.44–0.76)	<0.0001	0.698 (0.587–0.827)	0.6500	0.0420	0.0032	15.21	15.21
Definition of Chen et al
Two-stage algorithm of the EWGSOP	3.39±0.702	19.8 (7.48–29.8)	<0.0001
SARC-F of Malmstrom et al	0.44±0.117	1.49 (1.18–1.87)	0.0006	0.821 (0.735–0.901)				2	2
Screening grid of Goodman et al	0.03±0.009	1.03 (1.01–1.05)	0.0007	0.710 (0.572–0.848)	0.2100			62.1	73.3
Score chart of Ishii et al	0.04±0.008	1.04 (1.03–1.06)	<0.0001	0.914 (0.873–0.956)	0.0200	0.0032		125.9	117.8
Equation of Yu et al	−0.36±0.127	0.70 (0.54–0.90)	0.0006	0.719 (0.592–0.856)	0.1900	0.9200	0.0001	15.21	16.58
Definition of Studenski et al
Two-stage algorithm of the EWGSOP	1.77±0.594	5.91 (1.83–19.0)	0.0027
SARC-F of Malmstrom et al	0.18±0.109	1.34 (1.13–1.60)	0.0008	0.688 (0.572–0.803)				2	4
Screening grid of Goodman et al	−0.02±0.009	0.98 (0.96–0.99)	0.0478	0.600 (0.488–0.712)	0.3400			24.2	43.7
Score chart of Ishii et al	0.05±0.010	1.05 (1.03–1.07)	<0.0001	0.891 (0.831–0.951)	0.0002	<0.0001		128.5	128.5
Equation of Yu et al	−0.29±0.117	0.75 (0.59–0.94)	0.0146	0.710 (0.572–0.841)	0.7800	0.2100	0.0010	14.1	14.1

Note:

a Covariates: age, sex, number of comorbidities, number of drugs and cognitive status included in the regression model.

Abbreviations: AUC, area under the curve; EWGSOP, European Working Group on Sarcopenia in Older People; OR, odds ratio.

Figure 2 ROC curves for comparisons of the five diagnostic definitions of sarcopenia.

Abbreviation: ROC, receiver operating characteristic.

Cruz-JentoftAJBaeyensJPBauerJMSarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older PeopleAge Ageing201039441242320392703

 PubMed Web of Science ®Google Scholar

FieldingRAVellasBEvansWJSarcopenia: an undiagnosed condition in older adults. current consensus definition: prevalence, etiology, and consequences. International Working Group on SarcopeniaJ Am Med Dir Assoc201112424925621527165

 PubMed Web of Science ®Google Scholar

MorleyJEAbbatecolaAMArgilesJMSarcopenia with limited mobility: an International ConsensusJ Am Med Dir Assoc201112640340921640657

 PubMed Web of Science ®Google Scholar

ChenL-KLiuL-KWooJSarcopenia in Asia: consensus Report of the Asian Working Group for SarcopeniaJ Am Med Dir Assoc20141529510124461239

 PubMed Web of Science ®Google Scholar

StudenskiSAPetersKWAlleyDEThe FNIH Sarcopenia Project: rationale, study description, conference recommendations, and final estimatesJ Gerontol A Biol Sci Med Sci201469554755824737557

 PubMed Web of Science ®Google Scholar

MalmstromTKMorleyJEHarenMTSARC-F: a simple questionnaire to rapidly diagnose sarcopeniaJ Am Med Dir Assoc201314853153223810110

 PubMed Web of Science ®Google Scholar

GoodmanMJGhateSRMavrosPDevelopment of a practical screening tool to predict low muscle mass using NHANES 1999–2004J Cachexia Sarcopenia Muscle20134318719723673689

 PubMed Web of Science ®Google Scholar

IshiiSTanakaTShibasakiKDevelopment of a simple screening test for sarcopenia in older adultsGeriatr Gerontol Int201414suppl 19310124450566

 PubMed Web of Science ®Google Scholar

YuSAppletonSChapmanIAn anthropometric prediction equation for appendicular skeletal muscle mass in combination with a measure of muscle function to screen for sarcopenia in primary and aged careJ Am Med Dir Assoc2015161253025239016

 PubMed Web of Science ®Google Scholar