Comparisons of sarcopenia prevalence based on different diagnostic criteria in Chinese older adults

Abstract

The study aimed to describe the prevalence of sarcopenia and discussed the applicability of different diagnostic criteria in Chinese older adults. 286 Chinese adults (136 men and 150 women) aged 60–88 were recruited. The prevalence of sarcopenia were calculated using different diagnostic criteria. Physical functioning was compared in sarcopenic and non-sarcopenic older adults. Compared with the standard of EWGSOP (European Working Group on Sarcopenia in Older People), the prevalence of sarcopenia was higher when the IWGS (International Working Group on Sarcopenia) standard was applied (Men: 7.4% vs. 0.8%; Women: 4.7% vs. 0%). If the AWGS (Aisa Working Group on Sarcopenia) standard was applied, the prevalence was 5.9% in men and 0.7% in women. In conclusion, the prevalence of sarcopenia in Chinese older adults ranged from 0% to around 10% when the diagnostic criteria of IGWS, EWGSOP and AGWS were applied. Further studies are still needed to investigate appropriate diagnostic criterion of sarcopenia for Chinese population.

Introduction

Sarcopenia, which is characterized by the decreased skeletal muscle mass and strength associated with aging, may lead to serious consequences, such as falls, fractures, physical disability and increased mortality (1, 2). The reported prevalence of sarcopenia in different regions ranged from about 10% to 50%, due to differences in the operational definition of sarcopenia, measurement techniques and study population (3, 4). Most studies in Asian populations showed that the prevalence of sarcopenia was lower than in white populations. In Hong Kong, 12.3% Chinese men and 7.6% women were found to be sarcopenic (5). The prevalence of sarcopenia in Korean older adults was 0.1% to around 10% using different criteria (6). Our previous study showed that very few Chinese adults could be classified as having sarcopenia (7).

A sarcopenia index proposed by Baumgartner and his colleagues defined sarcopenia as relative appendicular skeletal muscle mass (RASM) being two standard deviations or lower than the mean of a healthy reference population (8). Using this index, Chinese adults were found to have approximately 15% lower RASM than their Western counterparts, which would suggest lower cutoff points and lower prevalence of sarcopenia (5, 7). However, lower prevalence of sarcopenia using this definition may not be associated with better strength and physical performance and lower disability, morbidity and mortality. Therefore, the widely-used definition for sarcopenia maybe not fit for Chinese older adults. In recent years, the European Working Group on Sarcopenia in Older People (EWGSOP), the International Working Group on Sarcopenia (IWGS) and Asia Working Group on Sarcopenia (AWGS) recommended their respective consensus definitions (9, 10, 11). The three working groups attached great importance to physical function and muscle strength. Several studies have investigated the prevalence of sarcopenia in different regions using the new consensus definitions (6, 12, 13). However, few studies reported the prevalence of sarcopenia using the new criteria in the Chinese older population.

Therefore, the purpose of this study is to describe the prevalence of sarcopenia and discuss the applicability of different diagnostic criteria in Chinese older adults.

Methods

Study Design and Participants

The data of this study came from a cross-sectional study on body composition in Chinese older adults at Hangzhou, Zhejiang Province in China in June 2013. Older adults aged at least 60 years old from 30 communities in Hangzhou were randomly invited to attend this research project. Ten participants were recruited from each community, so that a total of 300 older adults participated in this study. Individuals with the following conditions were excluded from the study: 1) unable to communicate with research tester; 2) have physical disability; 3) received medications that may influence their body composition; 4) with a mechanical implant in his/her body. Participants were required to complete a series of tests including body composition, hand grip, gait speed, et al. and a questionnaire about their health status and physical functioning. Two participants with physical disabilities or who have received medications that may influence their body composition were excluded from the survey. Twelve participants were excluded because of incomplete data. Consequently, 286 participants (136 men and 150 women) aged 60-88 were included in the data analysis. Signed informed consent was obtained from all participants prior to the survey. The study was approved by the institutional review board of Zhejiang Institute of Sports Science.

Body Composition

Participants’ whole and regional body lean mass were measured by a Norland XR-800 densitometer machine. Appendicular skeletal muscle mass (ASM) was calculated as the sum of lean mass in arms and legs (14). RASM was calculated based on the equation (RASM =ASM/height²). Skeletal muscle index (SMI) was calculated based on the equation (SMI=100×skeletal muscle mass/body mass)(15).

Muscle strength and gait speed

Hand grip strength was measured by a standard adjustable digital handgrip dynamometer (Beijing Xindong Scientific Instruments Co., LTD, China). Participants were instructed to stand up and exert maximal force with shoulder adducted and neutrally rotated and elbow in full extension. Each participant was allowed to take one test trial, followed by three test measurements for each side, and the maximum value of the dominant hand was used in the data analysis. As was suggested by previous studies (9, 16), hand grip strength lower than 20kg in women and 30kg in men was defined as hand grip weakness. Participants’ gait speed was tested in a 6 meter course. Participants were informed to walk at their usual pace and walking time was timed with a stopwatch. Participants could use a walking aid if they were accustomed to use it. Low gait speed was define as gait speed lower than 0.8 m/s (9).

Physical functioning and other information

Participants’ self-reported physical functioning was measured by the 36-Item Short Form Health Survey (SF-36) questionnaire with the assistance of trained testers. Physical functions tested included jogging, climbing stairs, walking, and some other basic skills which could ensure older people could function independently. The participants who reported to have limitations in a specific activity, regardless of the degree of limitation, were classified as having limitations in the activity. SF-36 demonstrated good validity and reliability and were widely applied in previous studies (17, 18). Participants’ demographic information was collected through a questionnaire.

Sarcopenia Classification

Five sets of criteria were used to indentify sarcopenia in this study. For the RASM method, class I sarcopenia was defined as the participants whose RASM were within one to two SDs below the sex-specific mean of young adults. Class II sarcopenia was defined as the participants whose RASM were lower than two SDs below the sex-specific mean of young adults. The data of the young reference population was based on a nationally representative survey in China (7). Similar to the RASM method, SMI class I sarcopenia was defined as the participants whose SMI were within one to two SDs below the sex-specific mean of young adults. SMI Class II sarcopenia was defined as the participants whose SMI were lower than two SDs below the sex-specific mean of young adults. The IWGS, EWGSOP and AWGS criteria, which include not only skeletal muscle mass but also muscle strength and physical performance, were well introduced by the three working groups (9, 10, 11). RASM of 7.23 kg/m² for men and 5.67 kg/m² for women, which were introduced by IGWS and RASM of 7.0 kg/m² for men and 5.4 kg/m² for women recommended by AGWS, were used as “absolute” cutoff points in the current study.

Data Analysis

Descriptive statistics (means, SDs and percentages) were used to describe key clinical and demographic characteristics. According to RASM, SMI, IWGS, EWGSOP and AWGS methods, the prevalence of sarcopenia in men and women were calculated respectively. A chi-squared test was applied to compare the percentages of participants having problems in physical functioning in sarcopenic and non-sarcopenic older adults. Logistic regression was applied to determine the odds ratios (OR) of having limitations in physical activities in sarcopenic older adults using non-sarcopenic older adults as reference. The 95% confidence interval (CI) is used to in the data analysis.

Results

A total of 286 participants (136 men and 150 women) were finally included in this study. The age of the study population ranged from 60 to 88 in men and 60 to 79 in women. Descriptive statistics of men and women are summarized in Table 1. Compared with women, men had more lean mass, lower body fat and better strength. However, no significant difference was found in gait speed or percentages of having problems in physical functioning in older men and women.

Table 1.

Characteristics of study population (mean±SD)

	Men, n=136	Women, n=150
Age (y)	66.5±4.8	65.4±45
Height (cm)	167.0±5.0*	1542±5.0*
Weight (kg)	65.4±9.3*	56.3±9.8*
BMI (kg/m2)	23.4±3.1	23.1±5.1
Total lean mass (kg)	45.4±5.5*	35.8±4.9*
Fat %	23.7±5.8*	36.1±5.6*
Fat mass (kg)	16.3±5.2*	21.8±5.9*
ALM (kg)	22.3±2.9*	16.4±2.6*
RASM (kg/m2)	8.0±0.9*	6.9±0.9*
SMI	72.4±5.4*	60.5±5.4*
Hand grip strength	38.4±7.8*	23.5±5.9*
Poor hand grip strength, %	12.7*	23.9*
Gait speed	1.1±0.3	1.1±0.26
Gait speed<0.8m/s, %	13.0	7.8
Gait speed<1m/s, %	42.3	32.0
Have limitations in the following activities
Vigorous activities, %	76.6	79.0
Moderate activities, %	23.2	24.5
Lifting or carrying groceries, %	23.0	25.4
Climbing several flights of stairs, %	40.8	40.6
Bending, kneeling or stooping, %	41.9	43.7
Walking more than one mile, %	27.0	31.2
Bathing or dressing by themselves, %	7.1	5.6

Note: *: gender difference p<0.05; Poor hand grip strength: man’s handgrip < 30kg; woman’s handgrip < 20kg; RASM: Relative Appendicular Skeletal Mass, =ASM/height²; SMI: Skeletal Muscle Index, =100×skeletal muscle mass/body mass

As it was showed in Table 2, using the RASM Class II sarcopenia standard (two SDs below the mean value of young adults), the cutoff points for Chinese population were 5.85 kg/m² and 4.23 kg/m². As a result, only 0.8% of men and none of women could be classified sarcopenic. The prevalence was increased to 11.4% and 0.7% if one SD standard was applied. Compared with RASM standards, using SMI as indicator, the prevalence of sarcopenia were higher in both men and women (Class II standard Men: 2.2% vs. 0.8%; Women: 7.5% vs. 0%; Class I standard men 22.2% vs. 11.4%, women 51.7% vs. 0.7%).

Table 2.

Prevalence of sarcopenia in Chinese older adults using different diagnostic criteria

Indicators & standard	Cutoff points	Men n=136	Women n=150
RASM Class I sarcopenia	M : RASM=6.91 kg/m2	11.4	0.7
	F : RASM=5.18kg/m2
RASM Class II sarcopenia	M : RASM=5.85kg/m2	0.8	0
	F : RASM=4.23kg/m2
SMI Class I sarcopenia	M : SMI =69	22.2	51.7
	F : SMI =60.4
SMI Class II sarcopenia	M : SMI =61.4	2.2	7.5
	F : SMI =53.4
IWGS	M: RASM=7.23 kg/m2	7.4	4.7
	F: RASM=5.67 kg/m2
EWGSOP	Gait speed < 1.0 m/s
	M : RASM=5.85kg/m2
	F : RASM=4.23kg/m2
	Gait speed < 0.8 m/s	0.8	0
	M : Hand grip strength < 30kg
	F : Hand grip strength< 20kg
AWGS	M: RASM=7.0 kg/m2
	F: RASM=5.3 kg/m2
	Gait speed < 0.8 m/s	5.9	0.7
	M : Hand grip strength < 26kg
	F : Hand grip strength < 18kg

Note: RASM: relative appendicular skeletal muscle mass; SMI: skeletal muscle index, 100×skeletal muscle mass/body mass; Class I: one SD below the mean value of young adults; Class II: two SDs below the mean value of young adults

Using the IWGS standard gave us a cutoff of 7.23 kg/m² in men and 5.67 kg/m² in women, which is higher than the cutoff points of EWGSOP (5.85 kg/m² in men and 4.23 kg/m² in women). Therefore, compared with the standard of EWGSOP, the prevalence of sarcopenia in the current study population was higher when the IWGS standard was applied (Men: 7.4% vs. 0.8%; Women: 4.7% vs. 0%). If the AWGS standard was applied, the prevalence of sarcopenia would be 5.9% in men and 0.7% in women.

Percentages of having physical difficulties in sarcopenic and non-sarcopenic older men and women defined by different criteria were summarized in Table 3 and Table 4. The data of percentages using several criteria (e.g. RASM class II) were not presented because prevalence of sarcopenia was very low (< 5%) so that none or only several participants could be included in the calculation. There were no significant difference in the percentages between sarcopenic and non-sarcopenic older adults in most groups using the criteria of RASM, SMI and IWGS. However, using the AWGS standard, significant differences were found in “low hand grip strength”, “low gait speed” and “lifting or carrying groceries” between the sarcopenic and non-sarcopenic men. Significant differences were also found in “low gait speed” and “climbing several flights of stairs” between the sarcopenic and non-sarcopenic women when IWGS standard was used. The results of logistic regression showed that when the AWGS standard was applied, sarcopenic older adults had significant higher odds to have low hand grip strength (OR=16.29, 95%CI: 3.53-75.15) and low gait speed (OR=5.57, 95%CI: 1.27-24.41) when compared with the non-sarcopenic study population (Table 5).

Table 3.

Percentages of having physical difficulties in sarcopenic and non-sarcopenic elder men defined by different criteria

	RASM Class I		SMI Class I		IWGS		AWGS
	Non-sarcopenic	Sarcopenic	Non-sarcopenic	Sarcopenic	Non-sarcopenic	Sarcopenic	Non-sarcopenic	Sarcopenic
	N=117	N=15	N=105	N=30	N=126	N=10	N=128	N=8
Low hand grip strength	10.1	28.6	10.0	20.0	12.1	20.0	9.3*	62.5*
Low gait speed	11.9	21.4	14.1	8.3	9.7*	50.0*	10.4*	50.0*
Having a little or serious difficulties in
Vigorous activities	77.4	64.3	76.5	76.0	77.2	70.0	76.7	75.0
Moderate activities	24.3	21.4	24.2	20.0	22.6	30.0	22.2	37.5
Lifting or carrying groceries	24.1	21.4	23.2	23.1	21.6	40.0	21.2#	50.0#
Climbing several flights of stairs	42.6	28.6	40.4	42.3	41.7	30.0	39.3	62.5
Bending, kneeling or stooping	44.3	28.6	46.4	26.9	41.2	50.0	42.2	37.5
Walking more than one mile	28.7	21.4	27.3	26.9	27.6	20.0	26.3	37.5
Bathing or dressing by themselves	8.3	0	8.0	3.8	6.9	10.0	7.6	0

Note: *: p<0.05, #:p<0.10

Table 4.

Percentages of having physical difficulties in sarcopenic and non-sarcopenic elder women defined by different criteria

	SMI Class I		SMI Class II		IWGS
	Non-sarcopenic	Sarcopenic	Non-sarcopenic	Sarcopenic	Non-sarcopenic	Sarcopenic
	N=71	N=76	N=136	N=11	N=143	N=7
Low hand grip strength	20.6	28.2	24.6	22.2	23.0	42.9
Low gait speed	3.2#	12.1#	8.3	0.0	5.8*	42.9*
Having a little or serious difficulties in
Vigorous activities	86.6#	72.6#	80.8	60.0	79.4	71.4
Moderate activities	25.4	24.6	24.6	30.0	23.5	42.9
Lifting or carrying groceries	28.4	23.6	25.6	30.0	25.2	28.6
Climbing several flights of stairs	41.2	41.7	40.8	40.0	39.0 #	71.4 #
Bending, kneeling or stooping	46.3	43.1	44.7	40.0	44.4	28.6
Walking more than one mile	37.3	26.8	32.8	20.0	30.6	42.9
Bathing or dressing by themselves	4.5	7.0	5.4	10.0	5.1	14.3

Note: *: p<0.05, #:p<0.10

Table 5.

Odds ratios of having physical difficulties in sarcopenic group using non-sarcopenia group as reference

	RASM Class I	SMI Class I	SMI Class II	IWGS	AWGS
	N=282	N=282	N=282	N=286	N=282
Poor hand grip strength	3.12 (0.86-11.32)	1.68 (0.86-3.27)	2.72 (0.73-10.15)	2.12(0.69-6.54)	16.29(3.53-75.15) **
Poor gait speed	2.04 (0.51-8.24)	1.41 (0.57-3.48)	Not available	10.38(3.46-31.16) **	5.57 (1.27-24.41)**
Having a little or serious difficulties in
Vigorous activities	0.59 (0.19-1.86)	0.60 (0.32-1.15)	0.40 (0.12-1.30)	0.66 (0.22-1.96)	0.95 (0.19-4.89)
Moderate activities	1.16 (0.34-3.92)	0.91 (0.49-1.69)	1.37 (0.40-4.65)	1.84(0.65-5.22)	1.84 (0.43-7.88)
Lifting or carrying groceries	1.16 (0.35-3.93)	0.86 (0.47-1.60)	1.31 (0.38-4.45)	1.82 (0.64-5.18)	3.25 (0.80-13.17)
Climbing several flights of stairs	0.67 (0.22-2.09)	1.05 (0.62-1.80)	1.21 (0.39-3.73)	1.32 (0.49-3.57)	2.10 (0.53-8.32)
Bending, kneeling or stooping	0.45 (0.14-1.49)	0.70 (0.41-1.20)	0.76 (0.24-2.42)	0.94 (0.34-2.56)	1.23 (0.31-4.87)
Walking more than one mile	0.91 (0.27-3.05)	0.73 (0.41-1.32)	0.64 (0.17-2.42)	1.04 (0.35-3.08)	1.49 (0.35-6.37)
Bathing or dressing by themselves	Not available	0.98 (0.33-2.93)	1.32 (0.16-10.99)	2.04(0.42-9.79)	0.79 (0.17-3.73)

Note: Age and gender were adjusted in the regression, **: p<0.01; The 95% confidence interval (CI) is used to used to estimate the precision of the OR.

Discussion

Using different definitions of sarcopenia, the prevalence of sarcopenia in the current study population was calculated. Similar to the results of previous studies, the results also showed that the prevalence varies greatly with different criteria. The prevalence ranged from 0% to around 10%, except for the prevalence of sarcopenia in women based on SMI method (Class I). The prevalence depended largely on the applied indicators and cutoff points. The cutoff points of RASM applied in the studies in Korea (men:7.40kg/m², women:5.14kg/m2) (19) and Taiwan (men:7.27kg/m², women:5.44kg/m²) (20) were roughly equivalent to the ones in the Rosetta study (men:7.26kg/m², women:5.5kg/m²) (8), Health ABC study (men:7.25kg/m², women:5.67kg/m²) (21) and in Italy (men:7.59kg/m², women: 5.47kg/m²) (22). In contrast, the cutoff values in the studies in Hong Kong (men: 5.72kg/m², women: 4.82kg/m²) (23) and mainland China (men:5.85kg/m², women:4.23kg/m²) (7) were obviously lower than the other five studies. Racial differences may partly explain the big gap in cutoff points among different study populations. However, the great differences in cutoff scores among East Asian populations make it very hard to compare the prevalence of sarcopenia in Korea, Hong Kong and mainland China. In 2010, experts from EWGSOP reached a consensus on the definition and diagnosis of sarcopenia. Physical performance was emphasized by both of the working groups. However, the evaluation of muscle mass was still based on the normative populations in the criteria of EWGSOP, which means the classification of sarcopenia still depends largely on which cutoff point and reference population is used.

Norm-referenced standards and cutoff points were widely applied in measurement and evaluation practice. When a good young reference population can be achieved, establishing norm-referenced standards and cutoff scores for the diagnosis of sarcopenia is relatively easy. However, one of the limitations of norm-referenced standards is that the interpretation depends on the data of the reference population (24, 25). The application of criterion-referenced standards may help us solve this limitation. Compared with the norm-referenced standards in which the evaluation of a test-taker’s competency was determined relative to the performance of other test-takers, the criterion-referenced standards compares the test-taker’s performance with an absolute criterion (25). Defining sarcopenia based on future risk of physical limitations could be more meaningful when compared using the data of a young reference population directly. In fact, in 2004, Janssen and his colleagues had raised this idea and determined the skeletal muscle cutoff scores related to elevated physical disability risk in older adults (26). The results of that study showed that women with RASM of 5.76-6.75 and ≤5.75 kg/m² and men with RASM of 8.51-10.75 and ≤8.50 kg/m² were found to be associated with moderate and high physical disability risk. However, these cutoff points were not widely applied to report the prevalence of sarcopenia, probably because bioimpedance rather than DXA was used to estimate skeletal muscle. A longitudinal study conducted by Woo in 2009 also investigated “absolute” cutoff values in the Chinese population (27). However, a U-shaped instead of linear relationship was found between RASM and physical limitations. The findings were confirmed in their follow-up study (28). Using the data of the present study, a U-shaped relationship between RASM and physical limitation was not found, which could be due to relatively small sample size.

“Absolute” cutoff points recommended by IGWS (RASM of 7.23 kg/m² for men and 5.67 kg/m² for women) and AGWS (RASM of 7.0 kg/m² for men and 5.4 kg/m² for women) were applied in the current study. The results suggested that, compared with other criteria, AGWS and IGWS standard could discriminate physical limitations such as “lifting or carrying groceries” in men and “climbing several flights of stairs” in women. However, no significant difference was found in other groups. Further studies are still needed to investigate the scientific evidence for the establishment of diagnostic criterion for sarcopenia in Chinese population, which is very important in clinical application.

Several limitations should be acknowledged in this study. One of the major limitations is relatively small sample size. Because of the difficulties in the recruitment of older adults, there were about 300 participants were included and most of them were no more than 75 years old. In addition, the study was conducted in Hangzhou and not nationally representative data. Nevertheless, the study still provides some valuable data for the establishing diagnostic criteria of sarcopenia for Asian older adults.

In conclusion, the prevalence of sarcopenia in Chinese older adults ranged from 0% to around 10% when the diagnostic criteria of IGWS, EWGSOP and AGWS were applied. Further studies are still needed to investigate appropriate diagnostic criterion of sarcopenia for Chinese population.

Conflict of interest: This study is based upon work funded by Zhejiang Provincial Natural Science Foundation of China under Grant No. LQ12C11001 and Research Project of Sports Bureau of Zhejiang Province 2103.

Ethical standards: All of the authors have compiled with the “Principles of the Ethical Practice of Public Health,” as outlined in A Code of Ethics for Public Health Thomas, et al. The study was approved by the institutional review board of Zhejiang Institute of Sports Science.

Acknowledgement: Assistance in English writing provided by Joshua Bocher, the Coordinator for the Asian Diabetes Prevention Initiative Website, was greatly appreciated.