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Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study
Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5
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Original article
Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study Li-Kuo Liu, MD a, b, c, Liang-Yu Chen, MD a, c, Kuo-Ping Yeh, MD a, c, Ming-Hsien Lin, MD a, c, An-Chun Hwang, MD a, c, d, Li-Ning Peng, MD a, c, d, *, Liang-Kung Chen, MD, PhD a, c, d a
Aging and Health Research Center, National Yang Ming University, Taipei, Taiwan Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Public Health, National Yang Ming University, Taipei, Taiwan d Institute of Biomedical Informatics, National Yang Ming University, Taipei, Taiwan b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 October 2013 Accepted 12 January 2014
Background: The prognostic significance of sarcopenia and sarcopenic obesity (SO) among older people remains controversial. The main aim of this study was to evaluate the mortality risk of sarcopenia and SO among men aged 75 years and older in Taiwan. Methods: This prospective cohort study recruited all residents of the Banciao Veterans Home, a veterans retirement community in Taipei City in northern Taiwan. For all study participants, the demographic profile, comorbid medical conditions, biochemical markers, handgrip strength and gait speed, sarcopenia, SO, and all-cause mortality were collected during a 3-year follow-up period. Results: In the study, 680 residents participated. The prevalence of sarcopenia and SO was 60.3% and 19.7%, respectively. During the study period, 140 (20.6%) deaths were identified. The diseased individuals were older, more prone to having diabetes mellitus and sarcopenia, had lower serum levels of total cholesterol and triglycerides, but had no difference in SO. Comparisons between different statuses of SO showed that age; diabetes mellitus; metabolic syndrome; body mass index; waist circumference; handgrip strength; gait speed; systolic blood pressure; fasting plasma glucose; serum levels of total cholesterol, triglyceride, high-density lipoprotein; and mortality were all significantly different between the groups. Sarcopenia [odds ratio (OR), 2.64; 95% confidence interval (C.I.), 1.687e4.135; p < 0.001], diabetes mellitus (OR, 1.70; 95% CI, 1.083e2.267; p ¼ 0.021) were independent risk factors for mortality; whereas the serum level of triglyceride was protective (OR, 0.99; 95% CI, 0.989e0.997; p ¼ 0.001). The Cox proportional hazard model confirmed that sarcopenia was significantly associated with mortality with or without obesity. Conclusions: The mortality risk of sarcopenia significantly outweighed the survival benefits of obesity in old age. The unfavorable impact of SO may eventually result from sarcopenia, but not obesity. Copyright Ó 2014, Asia Pacific League of Clinical Gerontology & Geriatrics. Published by Elsevier Taiwan LLC. All rights reserved.
Keywords: All-cause mortality Elderly Frailty Sarcopenia Sarcopenic obesity
1. Introduction Sarcopenia, the age-related loss of skeletal muscle and decline in muscle strength,1,2 is reportedly associated with a number of adverse clinical outcomes such as physical disability, falls, fractures, frailty, extended hospitalization, infectious and noninfectious complications at hospital admissions, and all-cause mortality.3e9 However, sarcopenia may sometimes coexist with an increase in fat mass [i.e., sarcopenic obesity (SO)], which suggests that the
* Corresponding author. Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Number 201, Section 2, Shih-Pai Road, Taipei 11217, Taiwan. E-mail address: [email protected] (L.-N. Peng).
confluence of the two individual body composition phenotypes may potentiate the mutually adverse health impacts,10,11 and that the prevalence of sarcopenia significantly increases with age.12e14 Sarcopenic obesity has attracted extensive research attention; however, a standardized diagnostic strategy is still lacking. Despite the lack of standardized diagnostic strategy, various health risks of SO have been demonstrated such as higher cardiovascular disease,15 lower physical function and cardiopulmonary fitness,16 physical disability,17 frailty and poorer quality of life,6,18 longer hospitalization,19 and higher mortality of patients with end-stage renal disease and tumor.20,21 Whether the abovementioned health impacts result from SO or sarcopenia per se nonetheless remains controversial. Among all
2210-8335/$ e see front matter Copyright Ó 2014, Asia Pacific League of Clinical Gerontology & Geriatrics. Published by Elsevier Taiwan LLC. All rights reserved. http://dx.doi.org/10.1016/j.jcgg.2014.01.002
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
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L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5
adverse health outcomes, the association between SO and mortality in otherwise healthy older adults remains unclear because the effects of obesity and sarcopenia on the mortality of the elderly seem to develop in opposite directions. Evidence suggests that the relationship between the body mass index (BMI) and mortality in the elderly is a U-shaped curve, whereas the risk of mortality rises only at extreme BMI values over 35e40 kg/m2.22,23 Jassen5 and colleagues moreover report that increased BMI was protective against mortality for people aged 65 years and older, after controlling for waist circumference (WC). However, increased WC was associated with mortality when controlling for BMI, which implied that BMI may represent lean body mass for individuals with an equivalent WC, and WC reflects fat mass for individuals with an equal BMI.24 This discovery indicates that adiposity may still play an unfavorable role in mortality among older people. The double health burden model of SO concerning the health of older people seems reasonable; however, rarely do studies really examine the combined effect of obesity and muscle mass or strength on mortality in the elderly, and data from The Third National Health and Nutrition Examination Survey clearly showed that SO was not associated with poor functioning.25,26 It has been hypothesized that obesity alone in old age may protect against mortality, but the risk of mortality may outweigh the protective effect if obesity is combined with low muscle strength.27 Therefore, the main purpose of this study was to evaluate the mortality impact of SO among Chinese men aged 75 years and older in Taiwan. 2. Methods 2.1. Participants This study invited all people to participate who were aged 75 years or older living in the Banciao Veterans Home (Taipei, Taiwan), a veterans retirement community that is similar to assisted living residences in the United States. Most Banciao Veterans Home residents were physically fit and cognitively intact.28e32 From March 2008 through July 2008, all residents who consented to participate in this study were enrolled, and then followed for 3 years. For all participants, the survival status was determined through personal interviews conducted by research nurses or obtained from the Veterans Affairs Welfare Registry, which is linked to the National Death Registry (Taipei, Taiwan) in a real-time manner. This study was approved by the Institutional Review Board of the National Yang Ming University (Taipei, Taiwan). 2.2. Data collection For all participants, demographic profile, medical history, smoking, physical activities, and alcohol consumption were collected by a self-administrated questionnaire. Health behaviors were also collected such as smoking, habitual alcohol use, and physical activities.31 Research nurses performed anthropometric measurements of all participants, including sitting blood pressure, body height and weight, WC, handgrip strength, and a 6-m walk. Handgrip strength was measured by a digital dynamometer (T.K.K.5401; Takei Scientific Instruments Co., Ltd., Niigata, Japan) when patients were placed in an upright position with the unsupported, dominant arm parallel to the body. The highest value of three repeated trials was recorded for further data analysis. Moreover, the usual gait speed was measured by a 6-m walk.32 For each participant, venous blood sampling was performed after a 10hour overnight fast. Serum levels of total cholesterol (TC), lowdensity lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), serum triglyceride (TG), and fasting blood
Table 1 Demographic characteristics of older men aged 75 years or older living in the Banciao Veterans Home in Taipei, Taiwan. Overall (N ¼ 680) Age (y) Height (cm) Weight (kg) Body mass index (kg/m2) Hypertension Diabetes mellitus Metabolic syndrome Current smoker Alcohol drinker Physically active Handgrip strength (kg) Gait speed (m/s) Sarcopenic obesity status Sarcopenia (), central obesity Sarcopenia (), central obesity Sarcopenia (þ), central obesity Sarcopenia (þ), central obesity All-cause mortality Cancer Cardiovascular disease Infectious disease Other
82.5 4.7 162.8 6.4 62.6 9.8 23.7 3.3 56.2 22.2 31.6 34.3 20.3 67.0 18.9 9.6 0.88 0.34 () (þ) () (þ)
24.7 15.0 40.6 19.7 20.6 2.9 5.4 9.1 3.1
Data are presented as mean SD or %.
glucose (FPG) were measured by an automated clinical analyzers (XE-2100; Sysmex, Kobe, Japan and ADVIA 1800; Siemens). 2.3. Definition of metabolic syndrome and sarcopenic obesity Metabolic syndrome (MS) was defined by the National Cholesterol Education Program Adult Treatment Panel III Guideline (ATPIII) criteria, which was modified by the International Diabetes Federation for Chinese males. The diagnostic criteria included: (1) fasting glucose level of 100 mg/dL or greater or drug treatment for an elevated glucose level; (2) serum triglyceride level of 150 mg/dL or greater or drug treatment for an elevated triglyceride level; (3) HDL-C level less than 40 mg/dL or drug treatment for a reduced HDL-C level; (4) systolic blood pressure 130 mmHg or greater or a diastolic blood pressure of 85 mmHg or greater, or drug treatment for hypertension; and (5) waist circumference of 90 cm or greater or a BMI of 25 kg/m2 or greater. In this study, SO was defined when patients concomitantly demonstrated central obesity (WC of 90 cm or greater) and sarcopenia (surrogated by low handgrip strength).27,33 Because WC is reportedly more associated with adverse outcomes than with BMI in this age group,24 we selected WC rather than BMI to surrogate adiposity in this study. However, the cutoff for handgrip strength was modified in accordance with data from a Taiwanese norm.34 Wu et al34 report that the handgrip strength was approximately 25% lower in men aged 65 years and older than in Caucasians of the same age and gender; therefore, the cutoff for low handgrip strength in this study was defined as less than 22.5 kg, according to the European consensus33 with modification for ethnic considerations. All patients were categorized into four groups, according to their SO status: (1) sarcopenia-negative and central obesitynegative; (2) sarcopenia-negative and central obesity-positive; (3) sarcopenia-positive and central obesity-negative; and (4) sarcopenia-positive and central obesity-positive (i.e., SO by our definition). 2.4. Data analysis In this study, continuous variables were expressed as the mean and the standard deviation, and categorical variables were
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5 Table 2 Comparison of the characteristics between older people aged 75 years old who died and people who survived during the follow-up period.
Age (y) Hypertension Diabetes mellitus Smoking Alcohol drinking Exercise Body mass index (kg/m2) Waist circumference (cm) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Fasting plasma glucose (mg/dL) Serum total cholesterol (mg/dL) Serum triglyceride (mg/dL) Serum HDL-C (mg/dL) Handgrip strength (Kg) Gait speed (m/s) Sarcopenia Sarcopenic obesity
Mortality (þ) (N ¼ 140)
Mortality () (N ¼ 540)
p
83.4 5.1 52.1 28.6 39.3 12.1 63.6 23.4 3.4 85.7 9.1 135.9 21.5 71.9 14.8 106.3 35.4 168.5 34.6 104.2 45.1 59.6 14.3 16.3 8.8 0.74 0.30 78.6 23.9
82.3 4.5 57.2 20.6 33.1 22.2 67.8 23.8 3.3 86.5 9.3 138.3 22.0 70.8 13.0 106.3 30.7 180.2 36.7 129.2 75.7 59.0 15.6 19.6 9.6 0.91 0.34 55.6 19.8
0.011 0.280 0.042 0.323 0.054 0.476 0.201 0.406 0.246 0.395 0.993 0.001 <0.001 0.667 <0.001 <0.001 <0.001 0.293
Data are presented as mean SD or %. HDL-C ¼ High-density lipoprotein cholesterol.
expressed by the total number and percentage. Comparisons between continuous variables were performed by using the Student t test. Comparisons between categorical variables were performed with the Chi-square test, when appropriate. One-way analysis of variance (ANOVA) was used to compare variables between the different statuses of SO and the Bonferroni test was used for post hoc analysis. Multivariate logistic regression was used to determine the independent risk factors for mortality by inputting all statistically significant factors in the univariate analysis. Cox proportional hazards regression analysis was used to compare the mortality risk of patients with different statuses of SO. All statistical analyses were performed by commercial software (SPSS version 17.0; SPSS Inc., Chicago, IL, USA). For all tests, p < 0.05 (two-tailed) was statistically significant. 3. Results The study enrolled 680 men with a mean age of 82.5 4.7 years (range, 75e102 years). Table 1 summarizes the demographic characteristics. The overall prevalence of sarcopenia and SO was 60.3% and 19.7%, respectively. At the end of the follow-up period,
3
140 (20.6%) deaths were identified; 62 (9.1%) deaths were caused by infectious diseases; 37 (5.4%) deaths, by cardiovascular disease; 20 (2.9%) deaths, by cancer; and 21 (3.1%) deaths, by other causes such as accidents or injuries. Table 2 compared the clinical characteristics between the diseased patients and the surviving patients. The comparison revealed that that the diseased patients were older, more prone to having diabetes mellitus and sarcopenia, had lower serum levels of TC and TG, whereas sarcopenic obesity was not significantly different between the groups. Table 3 summarizes the comparison between participants with different statuses of SO. The comparison showed that age, diabetes mellitus, MS, BMI, WC, handgrip strength, gait speed, systolic blood pressure, FPG, serum levels of TC, TG, HDL-C, and mortality were all significantly different between the groups. In particular, the mortality rate was highest in the sarcopenia-positive and central obesity-negative groupsdeven more so than in the SO group (28.3% vs. 23.9%, p ¼ 0.042). Cardiometabolic characteristics were poorer in the SO group; however, the mortality risk was highest among sarcopenia-positive and central obesity-negative patients (Table 3). Multivariate logistic regression showed that sarcopenia (OR ¼ 2.64; 95% C.I., 1.687e4.135; p < 0.001) and diabetes mellitus (OR ¼ 1.70; 95% C.I., 1.083e2.267; p ¼ 0.021) were independent risk factors for mortality; but the serum level of TG was a protective factor (OR ¼ 0.99; 95% C.I, 0.989e0.997; p ¼ 0.001; Table 4). Cox proportional hazards regression was used to compare the mortality risk among patients with different statuses of SO. It indicated that sarcopenia rather than SO tended to have a stronger impact on mortality (Fig. 1). 4. Discussion Sarcopenic obesity, a confluence of two common phenotypes of aging-related changes in body composition, has gained extensive research attention internationally. Sarcopenic obesity has been associated with several adverse health outcomes, but the impact of SO on mortality in the older population remains controversial. Previous studies suggest that obesity may have a protective role against mortality in older adults,22,23 but the protective effect may be counteracted if obesity is combined with low muscle strength.27 Therefore, the unfavorable clinical outcomes of SO may have resulted from sarcopenia with or without the coexistence of obesity. In this study, patients were categorized into four groups in accordance with their SO status, and comparisons between the
Table 3 Comparison of the demographic characteristics between older people aged 75 years and older and different statuses of sarcopenic obesity.
Age (y) Hypertension Diabetes mellitus Metabolic syndrome Body mass index (kg/m2) Waist circumference (cm) Handgrip strength (cm) Gait speed (m/s) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Fasting plasma glucose (mg/dL) Serum total cholesterol (mg/dL) Serum triglyceride (mg/dL) Serum HDL-C (mg/dL) Mortality
Sarcopenia () Central obesity () (N ¼ 168)
Sarcopenia () Central obesity (þ) (N ¼ 102)
Sarcopenia (þ) Central obesity () (N ¼ 276)
Sarcopenia (þ) Central obesity (þ) (N ¼ 134)
p
82.0 4.5 52.3 14.3 12.5 22.5 2.5 81.6 5.9 27.0 3.4 1.0 0.3 140.3 23.1 70.3 14.1 102.7 22.7 182.8 37.5 118.6 72.9 61.7 17.1 8.9
81.5 4.3 63.7 28.4 76.5 26.5 2.8 96.7 6.2 28.2 3.8 1.0 0.3 140.1 19.6 72.2 11.4 115.7 42.0 183.1 37.0 143.4 75.7 56.2 14.5 14.7
83.1 4.8 54.7 19.9 13.4 22.2 2.7 80.7 6.2 13.1 7.8 0.8 0.3 134.2 22.2 70.7 13.8 103.0 29.6 174.6 36.8 111.7 53.0 60.4 15.4 28.3
82.6 4.7 58.2 32.1 63.8 26.6 2.5 95.6 4.4 13.5 8.2 0.7 0.3 140.6 20.3 71.8 13.0 110.4 34.8 174.1 33.8 141.9 89.9 55.3 12.3 23.9
0.01 0.283 0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.004 0.589 0.001 0.033 <0.001 <0.001 <0.001
Data are presented as mean SD or %. HDL-C ¼ high-density lipoprotein cholesterol.
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
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L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5
Table 4 Independent risk factors for mortality among older men aged 75 years and older.
Sarcopenia (surrogated by low handgrip strength) Age Diabetes mellitus Serum total cholesterol Serum triglyceride
Odds ratio
95% Confidence interval
p
2.64
1.687e4.135
<0.001
1.08 1.70 1.00 0.99
0.929e1.007 1.083e2.667 0.999e1.010 0.989e0.997
0.108 0.021 0.130 0.001
groups showed significant differences in cardiometabolic profiles, muscle strength, and physical performance. A recent study described gender-specific changes in body composition with relation to frailty. It showed that physical frailty was associated with loss of muscle mass in older men, but was attributed to fat percentage in women.35 Compared to nonsarcopenic patients, sarcopenic patients with or without central obesity were more likely to die during the study period. By contrast, sarcopenic nonobese patients were at a significantly higher risk of dying, compared to the SO patients. Therefore, the results of this study supported the principle that obesity in the elderly was protective against mortality and that the protective effect may persist with sarcopenia. However, the mortality risk of sarcopenia may outweigh the protective effect of obesity among older men. In this study, the prevalence of sarcopenia was as high as 60.3%, and the prevalence of SO was 19.7%. Because of the lack of muscle mass measurements, sarcopenia in this study was surrogated by handgrip strength, as in other studies.33 The prevalence of sarcopenia in this study was eventually compatible with a previous report in this age group in which more than 50% of Hispanic and non-Hispanic men over 80 years were sarcopenic.36 The mean age of our study cohort was 82.5 years. Therefore, we assumed that the adjusted cutoff of handgrip strength was satisfactory as the surrogate indicator of sarcopenia. Matching the proposed screening cutoff of gait speed (0.8 m/second) in a European consensus, the mean gait speed of sarcopenic patients in the current study was 0.7e0.8 m/second. The estimated prevalence of sarcopenia in this study was comparable to data from Westerners, although studies of muscle mass measurement and its associative factors are still needed because of the differences in ethnic backgrounds.37e39
Despite the extensive research effort, there are several limitations in this study. First, the study participants were selected from the Banciao Veterans Home (Taipei, Taiwan), a veterans retirement community. All participants were males. The extrapolation of the study results may be limited; however, the mortality risk of SO in older adults internationally was unclear. Most previous studies confirmed the association between SO and mortality were limited only to particular diseases.20,21 To the best of our knowledge, this is the first study evaluating the mortality impact of SO on the Chinese population, which may broaden our understanding of SO in different ethnic backgrounds. Second, because of the eligibility criteria for the veterans home admissions, all participants were homogenous in their demographic characteristics. However, homogeneity may help lessen confounding factors in data analysis (e.g., social vulnerability) because the study participants were universally low in their social engagement.30 Third, this study lacked precise measurements of the study participants’ body composition, including muscle mass and fat mass. However, as previously stated, the adjusted cutoff for handgrip strength corresponded favorably with gait speed. Therefore, we believe the adjusted handgrip strength sufficiently surrogated the diagnosis of sarcopenia. In conclusion, sarcopenia was a highly prevalent condition among older men living in a veterans home. During the 3-year follow-up period, sarcopenia, but not sarcopenic obesity, significantly predicted all-cause mortality. The clinical significance of sarcopenic obesity should be reevaluated because sarcopenia per se was a strong risk factor for mortality, whereas central obesity was protective against it. The survival benefits of obesity were lost when sarcopenia was present. Conflicts of interest The authors have no conflicts of interest to report relevant to this article. Acknowledgments This study was supported by the Veteran Affairs Commission, Executive Yuan, the Republic of China (Taipei, Taiwan) and by the Aging and Health Research Center of National Yang Ming University (Taipei, Taiwan). References
Fig. 1. Survival analysis of older people aged 75 years and older with different statuses of sarcopenic obesity.
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Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
Contents lists available at ScienceDirect
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Original article
Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study Li-Kuo Liu, MD a, b, c, Liang-Yu Chen, MD a, c, Kuo-Ping Yeh, MD a, c, Ming-Hsien Lin, MD a, c, An-Chun Hwang, MD a, c, d, Li-Ning Peng, MD a, c, d, *, Liang-Kung Chen, MD, PhD a, c, d a
Aging and Health Research Center, National Yang Ming University, Taipei, Taiwan Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Public Health, National Yang Ming University, Taipei, Taiwan d Institute of Biomedical Informatics, National Yang Ming University, Taipei, Taiwan b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 October 2013 Accepted 12 January 2014
Background: The prognostic significance of sarcopenia and sarcopenic obesity (SO) among older people remains controversial. The main aim of this study was to evaluate the mortality risk of sarcopenia and SO among men aged 75 years and older in Taiwan. Methods: This prospective cohort study recruited all residents of the Banciao Veterans Home, a veterans retirement community in Taipei City in northern Taiwan. For all study participants, the demographic profile, comorbid medical conditions, biochemical markers, handgrip strength and gait speed, sarcopenia, SO, and all-cause mortality were collected during a 3-year follow-up period. Results: In the study, 680 residents participated. The prevalence of sarcopenia and SO was 60.3% and 19.7%, respectively. During the study period, 140 (20.6%) deaths were identified. The diseased individuals were older, more prone to having diabetes mellitus and sarcopenia, had lower serum levels of total cholesterol and triglycerides, but had no difference in SO. Comparisons between different statuses of SO showed that age; diabetes mellitus; metabolic syndrome; body mass index; waist circumference; handgrip strength; gait speed; systolic blood pressure; fasting plasma glucose; serum levels of total cholesterol, triglyceride, high-density lipoprotein; and mortality were all significantly different between the groups. Sarcopenia [odds ratio (OR), 2.64; 95% confidence interval (C.I.), 1.687e4.135; p < 0.001], diabetes mellitus (OR, 1.70; 95% CI, 1.083e2.267; p ¼ 0.021) were independent risk factors for mortality; whereas the serum level of triglyceride was protective (OR, 0.99; 95% CI, 0.989e0.997; p ¼ 0.001). The Cox proportional hazard model confirmed that sarcopenia was significantly associated with mortality with or without obesity. Conclusions: The mortality risk of sarcopenia significantly outweighed the survival benefits of obesity in old age. The unfavorable impact of SO may eventually result from sarcopenia, but not obesity. Copyright Ó 2014, Asia Pacific League of Clinical Gerontology & Geriatrics. Published by Elsevier Taiwan LLC. All rights reserved.
Keywords: All-cause mortality Elderly Frailty Sarcopenia Sarcopenic obesity
1. Introduction Sarcopenia, the age-related loss of skeletal muscle and decline in muscle strength,1,2 is reportedly associated with a number of adverse clinical outcomes such as physical disability, falls, fractures, frailty, extended hospitalization, infectious and noninfectious complications at hospital admissions, and all-cause mortality.3e9 However, sarcopenia may sometimes coexist with an increase in fat mass [i.e., sarcopenic obesity (SO)], which suggests that the
* Corresponding author. Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Number 201, Section 2, Shih-Pai Road, Taipei 11217, Taiwan. E-mail address: [email protected] (L.-N. Peng).
confluence of the two individual body composition phenotypes may potentiate the mutually adverse health impacts,10,11 and that the prevalence of sarcopenia significantly increases with age.12e14 Sarcopenic obesity has attracted extensive research attention; however, a standardized diagnostic strategy is still lacking. Despite the lack of standardized diagnostic strategy, various health risks of SO have been demonstrated such as higher cardiovascular disease,15 lower physical function and cardiopulmonary fitness,16 physical disability,17 frailty and poorer quality of life,6,18 longer hospitalization,19 and higher mortality of patients with end-stage renal disease and tumor.20,21 Whether the abovementioned health impacts result from SO or sarcopenia per se nonetheless remains controversial. Among all
2210-8335/$ e see front matter Copyright Ó 2014, Asia Pacific League of Clinical Gerontology & Geriatrics. Published by Elsevier Taiwan LLC. All rights reserved. http://dx.doi.org/10.1016/j.jcgg.2014.01.002
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
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L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5
adverse health outcomes, the association between SO and mortality in otherwise healthy older adults remains unclear because the effects of obesity and sarcopenia on the mortality of the elderly seem to develop in opposite directions. Evidence suggests that the relationship between the body mass index (BMI) and mortality in the elderly is a U-shaped curve, whereas the risk of mortality rises only at extreme BMI values over 35e40 kg/m2.22,23 Jassen5 and colleagues moreover report that increased BMI was protective against mortality for people aged 65 years and older, after controlling for waist circumference (WC). However, increased WC was associated with mortality when controlling for BMI, which implied that BMI may represent lean body mass for individuals with an equivalent WC, and WC reflects fat mass for individuals with an equal BMI.24 This discovery indicates that adiposity may still play an unfavorable role in mortality among older people. The double health burden model of SO concerning the health of older people seems reasonable; however, rarely do studies really examine the combined effect of obesity and muscle mass or strength on mortality in the elderly, and data from The Third National Health and Nutrition Examination Survey clearly showed that SO was not associated with poor functioning.25,26 It has been hypothesized that obesity alone in old age may protect against mortality, but the risk of mortality may outweigh the protective effect if obesity is combined with low muscle strength.27 Therefore, the main purpose of this study was to evaluate the mortality impact of SO among Chinese men aged 75 years and older in Taiwan. 2. Methods 2.1. Participants This study invited all people to participate who were aged 75 years or older living in the Banciao Veterans Home (Taipei, Taiwan), a veterans retirement community that is similar to assisted living residences in the United States. Most Banciao Veterans Home residents were physically fit and cognitively intact.28e32 From March 2008 through July 2008, all residents who consented to participate in this study were enrolled, and then followed for 3 years. For all participants, the survival status was determined through personal interviews conducted by research nurses or obtained from the Veterans Affairs Welfare Registry, which is linked to the National Death Registry (Taipei, Taiwan) in a real-time manner. This study was approved by the Institutional Review Board of the National Yang Ming University (Taipei, Taiwan). 2.2. Data collection For all participants, demographic profile, medical history, smoking, physical activities, and alcohol consumption were collected by a self-administrated questionnaire. Health behaviors were also collected such as smoking, habitual alcohol use, and physical activities.31 Research nurses performed anthropometric measurements of all participants, including sitting blood pressure, body height and weight, WC, handgrip strength, and a 6-m walk. Handgrip strength was measured by a digital dynamometer (T.K.K.5401; Takei Scientific Instruments Co., Ltd., Niigata, Japan) when patients were placed in an upright position with the unsupported, dominant arm parallel to the body. The highest value of three repeated trials was recorded for further data analysis. Moreover, the usual gait speed was measured by a 6-m walk.32 For each participant, venous blood sampling was performed after a 10hour overnight fast. Serum levels of total cholesterol (TC), lowdensity lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), serum triglyceride (TG), and fasting blood
Table 1 Demographic characteristics of older men aged 75 years or older living in the Banciao Veterans Home in Taipei, Taiwan. Overall (N ¼ 680) Age (y) Height (cm) Weight (kg) Body mass index (kg/m2) Hypertension Diabetes mellitus Metabolic syndrome Current smoker Alcohol drinker Physically active Handgrip strength (kg) Gait speed (m/s) Sarcopenic obesity status Sarcopenia (), central obesity Sarcopenia (), central obesity Sarcopenia (þ), central obesity Sarcopenia (þ), central obesity All-cause mortality Cancer Cardiovascular disease Infectious disease Other
82.5 4.7 162.8 6.4 62.6 9.8 23.7 3.3 56.2 22.2 31.6 34.3 20.3 67.0 18.9 9.6 0.88 0.34 () (þ) () (þ)
24.7 15.0 40.6 19.7 20.6 2.9 5.4 9.1 3.1
Data are presented as mean SD or %.
glucose (FPG) were measured by an automated clinical analyzers (XE-2100; Sysmex, Kobe, Japan and ADVIA 1800; Siemens). 2.3. Definition of metabolic syndrome and sarcopenic obesity Metabolic syndrome (MS) was defined by the National Cholesterol Education Program Adult Treatment Panel III Guideline (ATPIII) criteria, which was modified by the International Diabetes Federation for Chinese males. The diagnostic criteria included: (1) fasting glucose level of 100 mg/dL or greater or drug treatment for an elevated glucose level; (2) serum triglyceride level of 150 mg/dL or greater or drug treatment for an elevated triglyceride level; (3) HDL-C level less than 40 mg/dL or drug treatment for a reduced HDL-C level; (4) systolic blood pressure 130 mmHg or greater or a diastolic blood pressure of 85 mmHg or greater, or drug treatment for hypertension; and (5) waist circumference of 90 cm or greater or a BMI of 25 kg/m2 or greater. In this study, SO was defined when patients concomitantly demonstrated central obesity (WC of 90 cm or greater) and sarcopenia (surrogated by low handgrip strength).27,33 Because WC is reportedly more associated with adverse outcomes than with BMI in this age group,24 we selected WC rather than BMI to surrogate adiposity in this study. However, the cutoff for handgrip strength was modified in accordance with data from a Taiwanese norm.34 Wu et al34 report that the handgrip strength was approximately 25% lower in men aged 65 years and older than in Caucasians of the same age and gender; therefore, the cutoff for low handgrip strength in this study was defined as less than 22.5 kg, according to the European consensus33 with modification for ethnic considerations. All patients were categorized into four groups, according to their SO status: (1) sarcopenia-negative and central obesitynegative; (2) sarcopenia-negative and central obesity-positive; (3) sarcopenia-positive and central obesity-negative; and (4) sarcopenia-positive and central obesity-positive (i.e., SO by our definition). 2.4. Data analysis In this study, continuous variables were expressed as the mean and the standard deviation, and categorical variables were
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5 Table 2 Comparison of the characteristics between older people aged 75 years old who died and people who survived during the follow-up period.
Age (y) Hypertension Diabetes mellitus Smoking Alcohol drinking Exercise Body mass index (kg/m2) Waist circumference (cm) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Fasting plasma glucose (mg/dL) Serum total cholesterol (mg/dL) Serum triglyceride (mg/dL) Serum HDL-C (mg/dL) Handgrip strength (Kg) Gait speed (m/s) Sarcopenia Sarcopenic obesity
Mortality (þ) (N ¼ 140)
Mortality () (N ¼ 540)
p
83.4 5.1 52.1 28.6 39.3 12.1 63.6 23.4 3.4 85.7 9.1 135.9 21.5 71.9 14.8 106.3 35.4 168.5 34.6 104.2 45.1 59.6 14.3 16.3 8.8 0.74 0.30 78.6 23.9
82.3 4.5 57.2 20.6 33.1 22.2 67.8 23.8 3.3 86.5 9.3 138.3 22.0 70.8 13.0 106.3 30.7 180.2 36.7 129.2 75.7 59.0 15.6 19.6 9.6 0.91 0.34 55.6 19.8
0.011 0.280 0.042 0.323 0.054 0.476 0.201 0.406 0.246 0.395 0.993 0.001 <0.001 0.667 <0.001 <0.001 <0.001 0.293
Data are presented as mean SD or %. HDL-C ¼ High-density lipoprotein cholesterol.
expressed by the total number and percentage. Comparisons between continuous variables were performed by using the Student t test. Comparisons between categorical variables were performed with the Chi-square test, when appropriate. One-way analysis of variance (ANOVA) was used to compare variables between the different statuses of SO and the Bonferroni test was used for post hoc analysis. Multivariate logistic regression was used to determine the independent risk factors for mortality by inputting all statistically significant factors in the univariate analysis. Cox proportional hazards regression analysis was used to compare the mortality risk of patients with different statuses of SO. All statistical analyses were performed by commercial software (SPSS version 17.0; SPSS Inc., Chicago, IL, USA). For all tests, p < 0.05 (two-tailed) was statistically significant. 3. Results The study enrolled 680 men with a mean age of 82.5 4.7 years (range, 75e102 years). Table 1 summarizes the demographic characteristics. The overall prevalence of sarcopenia and SO was 60.3% and 19.7%, respectively. At the end of the follow-up period,
3
140 (20.6%) deaths were identified; 62 (9.1%) deaths were caused by infectious diseases; 37 (5.4%) deaths, by cardiovascular disease; 20 (2.9%) deaths, by cancer; and 21 (3.1%) deaths, by other causes such as accidents or injuries. Table 2 compared the clinical characteristics between the diseased patients and the surviving patients. The comparison revealed that that the diseased patients were older, more prone to having diabetes mellitus and sarcopenia, had lower serum levels of TC and TG, whereas sarcopenic obesity was not significantly different between the groups. Table 3 summarizes the comparison between participants with different statuses of SO. The comparison showed that age, diabetes mellitus, MS, BMI, WC, handgrip strength, gait speed, systolic blood pressure, FPG, serum levels of TC, TG, HDL-C, and mortality were all significantly different between the groups. In particular, the mortality rate was highest in the sarcopenia-positive and central obesity-negative groupsdeven more so than in the SO group (28.3% vs. 23.9%, p ¼ 0.042). Cardiometabolic characteristics were poorer in the SO group; however, the mortality risk was highest among sarcopenia-positive and central obesity-negative patients (Table 3). Multivariate logistic regression showed that sarcopenia (OR ¼ 2.64; 95% C.I., 1.687e4.135; p < 0.001) and diabetes mellitus (OR ¼ 1.70; 95% C.I., 1.083e2.267; p ¼ 0.021) were independent risk factors for mortality; but the serum level of TG was a protective factor (OR ¼ 0.99; 95% C.I, 0.989e0.997; p ¼ 0.001; Table 4). Cox proportional hazards regression was used to compare the mortality risk among patients with different statuses of SO. It indicated that sarcopenia rather than SO tended to have a stronger impact on mortality (Fig. 1). 4. Discussion Sarcopenic obesity, a confluence of two common phenotypes of aging-related changes in body composition, has gained extensive research attention internationally. Sarcopenic obesity has been associated with several adverse health outcomes, but the impact of SO on mortality in the older population remains controversial. Previous studies suggest that obesity may have a protective role against mortality in older adults,22,23 but the protective effect may be counteracted if obesity is combined with low muscle strength.27 Therefore, the unfavorable clinical outcomes of SO may have resulted from sarcopenia with or without the coexistence of obesity. In this study, patients were categorized into four groups in accordance with their SO status, and comparisons between the
Table 3 Comparison of the demographic characteristics between older people aged 75 years and older and different statuses of sarcopenic obesity.
Age (y) Hypertension Diabetes mellitus Metabolic syndrome Body mass index (kg/m2) Waist circumference (cm) Handgrip strength (cm) Gait speed (m/s) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Fasting plasma glucose (mg/dL) Serum total cholesterol (mg/dL) Serum triglyceride (mg/dL) Serum HDL-C (mg/dL) Mortality
Sarcopenia () Central obesity () (N ¼ 168)
Sarcopenia () Central obesity (þ) (N ¼ 102)
Sarcopenia (þ) Central obesity () (N ¼ 276)
Sarcopenia (þ) Central obesity (þ) (N ¼ 134)
p
82.0 4.5 52.3 14.3 12.5 22.5 2.5 81.6 5.9 27.0 3.4 1.0 0.3 140.3 23.1 70.3 14.1 102.7 22.7 182.8 37.5 118.6 72.9 61.7 17.1 8.9
81.5 4.3 63.7 28.4 76.5 26.5 2.8 96.7 6.2 28.2 3.8 1.0 0.3 140.1 19.6 72.2 11.4 115.7 42.0 183.1 37.0 143.4 75.7 56.2 14.5 14.7
83.1 4.8 54.7 19.9 13.4 22.2 2.7 80.7 6.2 13.1 7.8 0.8 0.3 134.2 22.2 70.7 13.8 103.0 29.6 174.6 36.8 111.7 53.0 60.4 15.4 28.3
82.6 4.7 58.2 32.1 63.8 26.6 2.5 95.6 4.4 13.5 8.2 0.7 0.3 140.6 20.3 71.8 13.0 110.4 34.8 174.1 33.8 141.9 89.9 55.3 12.3 23.9
0.01 0.283 0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.004 0.589 0.001 0.033 <0.001 <0.001 <0.001
Data are presented as mean SD or %. HDL-C ¼ high-density lipoprotein cholesterol.
Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002
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L.-K. Liu et al. / Journal of Clinical Gerontology & Geriatrics xxx (2014) 1e5
Table 4 Independent risk factors for mortality among older men aged 75 years and older.
Sarcopenia (surrogated by low handgrip strength) Age Diabetes mellitus Serum total cholesterol Serum triglyceride
Odds ratio
95% Confidence interval
p
2.64
1.687e4.135
<0.001
1.08 1.70 1.00 0.99
0.929e1.007 1.083e2.667 0.999e1.010 0.989e0.997
0.108 0.021 0.130 0.001
groups showed significant differences in cardiometabolic profiles, muscle strength, and physical performance. A recent study described gender-specific changes in body composition with relation to frailty. It showed that physical frailty was associated with loss of muscle mass in older men, but was attributed to fat percentage in women.35 Compared to nonsarcopenic patients, sarcopenic patients with or without central obesity were more likely to die during the study period. By contrast, sarcopenic nonobese patients were at a significantly higher risk of dying, compared to the SO patients. Therefore, the results of this study supported the principle that obesity in the elderly was protective against mortality and that the protective effect may persist with sarcopenia. However, the mortality risk of sarcopenia may outweigh the protective effect of obesity among older men. In this study, the prevalence of sarcopenia was as high as 60.3%, and the prevalence of SO was 19.7%. Because of the lack of muscle mass measurements, sarcopenia in this study was surrogated by handgrip strength, as in other studies.33 The prevalence of sarcopenia in this study was eventually compatible with a previous report in this age group in which more than 50% of Hispanic and non-Hispanic men over 80 years were sarcopenic.36 The mean age of our study cohort was 82.5 years. Therefore, we assumed that the adjusted cutoff of handgrip strength was satisfactory as the surrogate indicator of sarcopenia. Matching the proposed screening cutoff of gait speed (0.8 m/second) in a European consensus, the mean gait speed of sarcopenic patients in the current study was 0.7e0.8 m/second. The estimated prevalence of sarcopenia in this study was comparable to data from Westerners, although studies of muscle mass measurement and its associative factors are still needed because of the differences in ethnic backgrounds.37e39
Despite the extensive research effort, there are several limitations in this study. First, the study participants were selected from the Banciao Veterans Home (Taipei, Taiwan), a veterans retirement community. All participants were males. The extrapolation of the study results may be limited; however, the mortality risk of SO in older adults internationally was unclear. Most previous studies confirmed the association between SO and mortality were limited only to particular diseases.20,21 To the best of our knowledge, this is the first study evaluating the mortality impact of SO on the Chinese population, which may broaden our understanding of SO in different ethnic backgrounds. Second, because of the eligibility criteria for the veterans home admissions, all participants were homogenous in their demographic characteristics. However, homogeneity may help lessen confounding factors in data analysis (e.g., social vulnerability) because the study participants were universally low in their social engagement.30 Third, this study lacked precise measurements of the study participants’ body composition, including muscle mass and fat mass. However, as previously stated, the adjusted cutoff for handgrip strength corresponded favorably with gait speed. Therefore, we believe the adjusted handgrip strength sufficiently surrogated the diagnosis of sarcopenia. In conclusion, sarcopenia was a highly prevalent condition among older men living in a veterans home. During the 3-year follow-up period, sarcopenia, but not sarcopenic obesity, significantly predicted all-cause mortality. The clinical significance of sarcopenic obesity should be reevaluated because sarcopenia per se was a strong risk factor for mortality, whereas central obesity was protective against it. The survival benefits of obesity were lost when sarcopenia was present. Conflicts of interest The authors have no conflicts of interest to report relevant to this article. Acknowledgments This study was supported by the Veteran Affairs Commission, Executive Yuan, the Republic of China (Taipei, Taiwan) and by the Aging and Health Research Center of National Yang Ming University (Taipei, Taiwan). References
Fig. 1. Survival analysis of older people aged 75 years and older with different statuses of sarcopenic obesity.
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Please cite this article in press as: Liu L-K, et al., Sarcopenia, but not sarcopenic obesity, predicts mortality for older old men: A 3-year prospective cohort study, Journal of Clinical Gerontology & Geriatrics (2014), http://dx.doi.org/10.1016/j.jcgg.2014.01.002