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Sarcopenia in chronic obstructive pulmonary disease: A study of prevalence and associated factors in the Southeast Asian population

Sarcopenia in chronic obstructive pulmonary disease: A study of prevalence and associated factors... Chronic obstructive pulmonary disease (COPD) has been described as a systemic disease. Sarcopenia is one of the systemic effects that is related to several adverse outcomes. The objectives of this study were to estimate the prevalence of sarcopenia and to determine the factors associated with sarcopenia in COPD patients in Southeast Asia. This was a cross-sectional study of COPD patients who attended a COPD clinic from May 2015 to December 2016. Baseline characteristics were collected and dual-energy X-ray absorptiometry was used to measure skeletal muscle mass. Handgrip strength was used to assess muscle strength, and as a measurement of physical performance, the 6-min walk distance was used. One hundred and twenty-one participants were recruited. Most of them were men (92.6%). Prevalence of sarcopenia was 24% (29 cases). Independent factors associated with sarcopenia were age  75 years (adjusted odds ratio (AOR) 13.3, severity of COPD (AOR 19.2 and 13.4 for moderate and severe COPD), Modified Medical Research Council (MMRC) scale (AOD 1.9), and obesity (AOR 0.04). Sarcopenia affects about one-quarter of COPD patients. Age, severity of COPD, MMRC scale, and BMI status were the factors associated with sarcopenia. Keywords Airway obstruction, body composition, fat-free mass index, lung disease, skeletal muscle mass Date received: 27 June 2017; accepted: 20 October 2017 1 Division of Geriatric Medicine, Department of Internal Medicine, Faculty of Medicine,KhonKaenUniversity, Khon Kaen, Thailand Department of Internal Medicine, Faculty of Medicine, Khon Introduction Kaen University, Khon Kaen, Thailand Chronic obstructive pulmonary disease (COPD) is Division of Respiratory System, Department of Internal Medicine, Faculty of Medicine,KhonKaenUniversity, Khon defined as a disease characterized by persistent air- Kaen, Thailand flow limitation that is usually progressive and associ- Division of Nuclear Medicine, Department of Radiology, Faculty ated with an enhanced chronic inflammatory response of Medicine, Khon Kaen University, Khon Kaen, Thailand in the airways and the lung to noxious particles or 5 Division of Ambulatory Medicine, Department of Internal gases. It can lead to substantial morbidity and pre- Medicine, Faculty of Medicine,KhonKaenUniversity, Khon mature death. It affects about 10% of general popula- Kaen, Thailand tion and about 50% of very heavy smokers. Aging is Corresponding author: an independent factor in the prevalence of COPD with Panita Limpawattana, Division of Geriatric Medicine, Department 14% in persons 65 years or over compared with 9.9% of Medicine, Faculty of Medicine, Khon Kaen University, Khon of younger persons. A doubling of the prevalence of Kaen 40002, Thailand. COPD was observed for every 10-year increment in Email: [email protected] Creative Commons CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). Limpawattana et al. 251 age. Existing reports show that COPD is not consi- severity of COPD and BMI is, however, inconsistent 16,17 dered only as a respiratory disease but also described with reports. as a systemic disease including weight loss and nutri- Regarding the current criteria for sarcopenia diag- tional abnormalities, skeletal muscle dysfunction, nosis, they incorporate muscle function which is mus- increased risk of cardiovascular disease, hormonal cle strength and/or physical performance. The and metabolic disturbances, osteoporosis, anxiety, prevalence of sarcopenia in COPD patients according 3–5 and depression. Therefore, a more holistic approach to that definition is limited. Additionally, associated of COPD is essential rather than focusing only on factors of sarcopenia in COPD particularly for the airflow limitations. outcomes involving the geriatric syndrome such as One of the systemic effects of COPD is sarcopenia. falling and disability have not been widely studied. This term has been described as an age-related decline Early detection of sarcopenia could facilitate the 6,7 in muscle mass and its function. This condition is implementation of interventions targeted at prevent- associated with unfavorable health outcomes such as ing the progression of sarcopenia and improving qual- falls, disability, hospitalization, poor quality of life, ity of life in patients with COPD. Therefore, the 8,9 and mortality. The etiology of sarcopenia is the primary objective of this study was to estimate the result of the physiologic changes in addition to the prevalence of sarcopenia in COPD patients and results of disease-related, nutrition, and activity. the secondary objective was to determine the factors Sarcopenia can be classified as physical frailty associated with sarcopenia in COPD patients. where frailty is associated with adverse health out- 11,12 comes. Sarcopenia was found to be associated Material and methods with worsening lung function in male COPD patients. COPD patients also have relative or an Study participants and setting absolute increase in fat mass which might contribute This was a cross-sectional study that was carried out to systemic inflammation, loss of fat-free mass, and with COPD patients who were 18 years old or over insulin resistance. Fat-free mass index, not body mass and attended COPD clinic of Srinagarind Hospital, index (BMI), was significantly related to pulmonary Khon Kaen, Thailand from May 2015 to December function, dyspnea severity, quality of life, and 14,15 2016. This COPD clinic is a tertiary care referral cen- reflected reduced skeletal muscle mass. Cur- ter of the university hospital which enrolled patients rently, the persons with COPD are recommended for from our internal medicine/family medicine clinic sarcopenia screening and assessment according to the and other community hospitals. Patients were recommendation of the Asian Working Group for Sar- 10 excluded if they had other active medical illnesses copenia (AWGS). such as heart failure functional class III–IV, pneumo- The prevalence of sarcopenia in COPD men older nia, septicemia, COPD exacerbation within the pre- than 40 years of age varies from 20% to 40% depend- ceding 4 weeks, patients who were unable to complete ing on age of studied population, gender, setting of 13,16 study due to physical limitations, patients who were population, and measurement methods. The pre- unwilling to participate in this study, and patients who valence of sarcopenia from existing reports in Asia is had limitations in performing dual energy X-ray 29.3% and for sarcopenic obesity is 14.2% ;how- absorptiometry (DXA) or conditions that would affect ever, the definition of sarcopenia from this study DXA results; history of barium taking or enemas over focused only on skeletal muscle mass. In a recent the past 2 weeks, patients who had metallic instru- study in the United Kingdom using the European mentation such as spinal fixation, patients with his- Working Group on Sarcopenia in Older People tory of a radionuclide scan over the past 2 weeks, and (EWGSOP) criteria which included either low mus- patients with a body weight over 200 kg (exceeded the cle strength or poor physical performance with low capacity). The study population was similar to the skeletal muscle mass, it was found at 14.5% among 17 previously published article. stable COPD patients in the outpatient setting. Fac- tors associated with sarcopenia in COPD patients in Definition literature review included age, nutritional status, exercise capacity, severity of COPD, functional per- COPD. COPD was diagnosed in patients according to formance, smoking status, comorbid diseases, and the criteria of the Global Initiative for Chronic Obstruc- self-reported hospital admission. The relation of tive Lung Disease (GOLD) that was characterized by 252 Chronic Respiratory Disease 15(3) persistent airflow limitation, a post-bronchodilator force handgrip strength and 6-MWD was used to measure expiratory volume in 1 s (FEV1) less than 70% of forced physical performance. vital capacity. Severity of COPD was classified into three groups: mild (FEV1>80% normal), moderate (FEV1 50– Procedure 79% normal), and severe (FEV1 <49% normal). For After consent, baseline patient data were collected by patients with severe COPD in this study, it included trained clinical researchers. The demographic infor- patients with severe COPD (FEV1 30–49% normal) and mation consisted of age, sex, educational level, smok- very severe COPD (FEV1 < 30% normal) based on the ing status, severity of COPD using the most recent GOLD staging system. report of pulmonary function tests within the past Sarcopenia. Criteria for sarcopenia diagnosis were 6 months (the patients were asked to take the deepest based on the definition of the AWGS which consists breath they could, and then exhaled into the sensor as of low muscle mass and low muscle strength and/or hard as possible, preferably at least 6 s), MMRC scale, poor physical performance. Skeletal muscle mass was underlying disease, regular medication uses, history estimated using DXA and appendicular skeletal mus- of falls over the past 12 months, self-report baseline cle mass index calculated as appendicular skeletal basic and instrumental activities of daily living (ADL) mass/height (ASMI). Handgrip strength was mea- using Barthel ADLs index and Chula index, history of sured using a handheld dynamometer and measure- nonelective admission over the past 12 months, ment of physical performance that used the 6-min weight, height, and systolic and diastolic blood pres- walk distance (6-MWD) according to the American sure at rest. Weight and height were used to calculate BMI, and systolic and diastolic blood pressures were Thoracic Society guidelines. The following cutoff presented as mean arterial blood pressure (MAP). values were used to identify sarcopenia; ASMI of 2 2 For sarcopenia diagnosis, muscle mass using DXA, 7.0 kg/m for men and 5.4 kg/m for women, and handgrip strength using grip dynamometer (it was either handgrip strength of <26 kg for men and <18 kg measured by asking the patients to hold the handgrip for women or a gait speed of <0.8 m/s. Pre- dynamometer in one hand, with the arm at right sarcopenia is defined as presence of low muscle mass angles and the elbow by the side of the body. When without influence on muscle strength or physical per- ready, the patients squeezed the dynamometer with formance and sarcopenic obesity is characterized by maximum isometric effort, which was maintained for the presence of sarcopenia according to the definition 2 20,21 of the AWGS with BMI > 25kg/m . about 5 s. Three attempts were tested and the maximal one was recorded), and physical performance using Modified Medical Research Council scale. The Modified the 6-MWD as previously described were performed 10,24,25 Medical Research Council (MMRC) scale was used to on all patients in the same period. evaluate dyspnea in daily living. It included five grades (0–4) of various physiological activities that provoke Sample size calculation dyspnea that was self-rated by the patient. The descrip- Sample size calculations were based on the primary tions were as follows: 0, not troubled with breathless- ness except with strenuous exercise; 1, troubled by objective of this study which was the estimated pre- shortness of breath when hurrying on the level or walk- valence of sarcopenia in COPD patients. As there was no study regarding the prevalence of sarcopenia in ing up a slight hill; 2, walked slower than people of the COPD patients according to the definition of the same age on the level because of breathlessness or has to AWGS, the estimated prevalence of 14.5% was stop for breath when walking at own pace on the level; 3, derived from an existing study. The estimation of stopped for breath after walking about 100 yards or after a population proportion with a specified absolute pre- a few minutes on the level; and 4, too breathless to leave cision formula was used to calculate this. At least 98 the house, or breathless when dressing or undressing. participants were sufficient to achieve the required sample size at the significance level of 0.05. Instruments Statistical analyses Muscle mass measurement used DXA (General Elec- tric (Lunar-Progidy) model). A grip dynamometer Descriptive statistics for baseline data were presented (GRIP-D (T.K.K.5401) model) was used to measure in percentage, mean, and standard deviation. If the Limpawattana et al. 253 Table 1. Baseline characteristics of studied population. distribution of these data was not a normal distribu- tion, then medians, and interquartile ranges were used Variables N ¼ 121 instead. Effects of factors associated with sarcopenia were evaluated using univariate and multivariate Age (years), mean (SD) 70 9.0 Age group (years), n (%) regressions analysis. For univariate analysis, crude <65 32 26.45 odds ratios (OR) and 95% confidence intervals (CIs) 65–74 47 38.84 were used to consider the strength of association 75 42 43.71 between factors associated with sarcopenia. Factors Male sex, n (%) 112 92.6 with a p < 0.20 or clinical significance in literature Educational level, n (%) review were then entered into a multiple logistic 6 years or lower 59 48.76 regression model. A value of p < 0.05 was considered 7–12 years 28 23.14 to indicate statistically significant differences, and >12 years 34 28.10 Smoking status, n (%) adjusted OR and their 95% CI were reported to con- Never smoker 7 5.79 sider the strength of association. All the data analyses Ex-smoker 104 85.95 were carried out using STATA version 10.0 (Stata- Current smoker 10 8.26 Corp, College Station, Texas, USA). Severity of COPD, n (%) Ethics approval was provided by the Ethics Com- Mild 31 25.62 mittee of the Faculty of Medicine, Khon Kaen Uni- Moderate 69 57.02 versity as instituted by the Helsinki Declaration. Severe 21 17.36 MMRC scale, mean (SD) 0.69 1.08 Comorbid diseases, n (%) Results Diabetes mellitus 12 9.92 Hypertension 46 38.02 Prevalence of sarcopenia among COPD patients Dyslipidemia 10 8.26 There were 121 participants with stable COPD Chronic arthritis 10 8.26 recruited in this study. Baseline characteristics of the Cancer 6 4.96 studied population are shown in Table 1. The majority Regular medication uses, n (%) Inhaled corticosteroid 113 93.39 of them were men (112 cases, 92.6%) with an age Systemic steroid 2 1.65 older than 65 years old (maximum age was 92 and Oral hypoglycemic drugs 7 5.79 minimum age was 47 years old). Most of them were Statin 13 10.74 ex-smokers with a moderate degree in severity of NSAIDs 1 0.83 COPD. Hypertension was the most common comor- History of fall at least two times over 3 0.89 bid disease. The overall ADL were well-preserved. the past 12 months, n (%) The distribution of low skeletal muscle mass, low Barthel scores, mean (SD) 19.9 1 handgrip strength, and walking speed is demonstrated Chula IADLs scores, mean (SD) 8.98 0.18 Nonelective admission over the past 32 26.45 in Figure 1. Low skeletal muscle mass was the main 12 months, n (%) component, followed by low handgrip strength. Low BMI (kg/m ), n (%) gait speed was found in the minority. According to the Underweight (<18.5) 19 15.7 definition of sarcopenia from the recommendation of Normal and over weight (18.5–24.9) 65 53.72 the AWGS, the prevalence of pre-sarcopenia was Obesity (>25) 37 30.58 about 15.7% (19 cases) and sarcopenia was 24% (29 MAP (mmHg), mean (SD) 95.96 10.68 cases); all of them were men and severe sarcopenia 6-MWD (m), mean (SD) 423.39 73.67 was found in about 2.5% (three cases). The preva- Gait speed (m/s), mean (SD) 1.18 0.2 Handgrip strength (kg), mean (SD) lence of sarcopenic obesity was 0.8% (one case). Male 26.65 6.02 Female 21.22 3.43 Factors associated with sarcopenia among Appendicular skeletal mass index (kg/m ), mean (SD) COPD patients Male 7.1 0.89 Female 6.25 0.46 Comparison of the risk factors between sarcopenic and nonsarcopenic patients with COPD using (continued) 254 Chronic Respiratory Disease 15(3) Table 1. (continued) Table 2. Factors associated with sarcopenia using univari- ate analyses. Variables N ¼ 121 Unadjusted p Osteoporosis, n (%) 45 37.19 Variables OR 95% CI Value Sarcopenia, n (%) 29 24 Age group (years) COPD: chronic obstructive pulmonary disease; NSAIDs: nonster- <65 1 — — oidal anti-inflammatory drugs; IADL: instrumental activities of 65–74 1.2 (0.3, 4.6) 0.8 daily living; BMI: body mass index; MAP: mean arterial blood pres- 75 5.3 (1.6, 17.7) <0.05 sure; SD: standard deviation; osteoporosis: defined when T-score Severity of COPD of femoral neck or lumbar spine 2.5 SD; 6-MWD: 6-min walk Mild 1 — — distance; MMRC scale: Modified Medical Research Council scale Moderate 3.3 (0.9, 12.2) 0.07 (it was available in 116 patients). Appendicular skeletal mass was calculated by summing the mus- Severe 5.7 (1.3, 25.3) <0.05 cle masses of the four limbs. MMRC scale 1.9 (1.3, 2.8) <0.05 Comorbid diseases Diabetes mellitus 1.1 (0.3, 4.2) 0.9 Hypertension 1.2 (0.5, 2.8) 0.7 Dyslipidemia 0.8 (0.2, 3.9) 0.8 Chronic arthritis 1 (omitted) Cancer 1.6 (0.3, 9.4) 0.6 Regular medication uses Inhaled corticosteroid 0.9 (0.2, 4.9) 0.9 Systemic steroid 3.3 (0.2, 53.7) 0.4 Oral hypoglycemic drugs 0.5 (0.1, 4.4) 0.5 Statin 1.5 (0.4, 5.2) 0.6 NSAIDs 1 (omitted) History of falls at least 1.6 (0.1, 18.4) 0.7 2 times over the past 12 months Barthel scores 1 (omitted) Chula IADLs scores 1 (omitted) Nonelective admission 2.0 (1.1, 3.7) <0.05 over the past 12 months BMI (kg/m ) Underweight 1 Figure 1. The relationship of low skeletal muscle mass, Normal and over weight 0.3 (0.1, 0.8) <0.05 Obesity 0.02 (002, 0.2) <0.05 low handgrip strength, and low gait speed in study populations. MAP (mmHg) 0.9 (0.9, 0.9) <0.05 Osteoporosis 1.8 (0.8, 4.3) 0.2 univariate analysis is shown in Table 2. For multivariate COPD: chronic obstructive pulmonary disease; OR: odds ratio; analysis, six factors where p < 0.2 or clinical signifi- CI: confidence interval; BMI: body mass index; MAP: mean arterial blood pressure; osteoporosis: defined when T-score of femoral cance from literature review from univariate analysis neck or lumbar spine 2.5 standard deviation; MMRC scale: were entered in the multiple regression models: age, Modified Medical Research Council scale; NSAIDs: nonsteroidal severity of COPD, MMRC scale, nonelective admission anti-inflammatory drugs; IADL: instrumental activities of daily over the past 12 months, BMI, MPA, and presence of living. osteoporosis (Table 3). After multicollinearity was checked, advanced age (>75 years), greater severity of prevalence of sarcopenia was about 1 in four of COPD, MMRC scale, and nonobese patients were the factors associated with sarcopenia in this study. all COPD patients. This finding was higher than pre- viously reported in the United Kingdom which was 14.5% but was comparable to the study in South 17,27 Discussion Korea which reported 25%. The possible expla- nations are the differences in body composition of This is the first study that examines sarcopenia in different ethnicities and Asian people appear to COPD using AWGS criteria in Southeast Asia. The Limpawattana et al. 255 Table 3. Factors associated with sarcopenia using multi- was very low in this study (0.8%). To the best of variate analyses. authors’ knowledge, there has been no study using similar criteria in COPD patients. The prevalence of Adjusted sarcopenic obesity in Asia in existing studies is about Variables OR 95% CI p Value 15%; however, this current study used only skeletal 13,32 Age group (years) muscle mass to detect sarcopenia. <65 1 — — There were four factors associated with sarcopenia 65–74 2.0 (0.4, 10.8) 0.4 using multivariate analyses: age, severity of COPD, 75 13.3 (2.2, 79.9) <0.05 MMRC scale, and BMI. Advancing age and severity Severity of COPD of COPD showed high magnitudes of associations. Mild 1 — — Commonly, a progressive loss of muscle mass occurs Moderate 19.2 (2.2, 166.4) <0.05 Severe 13.4 (1.2, 148.6) <0.05 at the age of 40 and is greater after 70 years. The MMRC scale 1.9 (1.1, 3.3) <0.05 decline in gait speed and grip strength was faster than 21,33 Nonelective admission 3.3 (0.8, 12.9) 0.1 muscle mass especially after the age of 70 years. over the past The result supports that age is one of the independent 12 months factors; however, only age >75 years showed statisti- BMI (kg/m ) cal significance. Because the patients in this study Underweight 1 — — were with age over than 40 years old, an age of Normal and over 1.6 (0.3, 7.9) 0.6 weight 65–74 years compared to an age of less than 65 years Obesity 0.04 (0.003, 0.6) <0.05 might not show the differences. For the severity of MAP (mmHg) 0.9 (0.9, 1.0) 0.1 COPD, it was consistent with the previous reports that Osteoporosis 1.4 (0.4, 5.1) 0.6 skeletal muscle masses were lower in a greater degree 14,17 of airflow limitation. This association might be COPD: chronic obstructive pulmonary disease; OR: odds ratio; CI: confidence interval; BMI: body mass index; MAP: mean arterial explained by (1) high resting energy expenditure as a blood pressure; osteoporosis: defined when T-score of femoral result of increased work of breathing and inadequate neck or lumbar spine 2.5 standard deviation; MMRC scale: dietary intake in severe COPD, (2) physical inactivity Modified Medical Research Council scale. due to exercise intolerance, (3) excessive apoptosis of skeletal muscle due to increased systemic inflamma- have a higher prevalence of sarcopenia than other tion, and (4) possible presence of hypoxia and the regions. Additionally, the variation of techniques more frequent use of systemic corticosteroids. Con- to estimate all parameters to diagnose sarcopenia is versely, severity of COPD showed no association with another reason. The study in the United Kingdom some reports; this might be due to the definition of diagnosed COPD using EWGSOP criteria and mea- sarcopenia that used low skeletal muscle mass alone sured skeletal muscle mass with bioelectrical impe- in that study while muscle strength and physical per- dance analysis (BIA) and quadriceps strength to formance were additional factors associated with evaluate muscle strength, whereas this study used severity of COPD did not measure. The MMRC DXA to measure skeletal muscle mass and handgrip scale increased the risk of sarcopenia. This finding 17,27 strength to rate muscle strength. Although BIA pre- was similar to the prior report. This scale had sents good reliability and correlation to DXA, BIA been widely studied regarding its correlation with underestimated muscle mass compared to DXA in pulmonary function tests. Additionally, it could pre- 29,30 22,35 prior studies. The study in Brazil regarding the dict morbidity and mortality in COPD patients. prevalence of sarcopenia in COPD using DXA was Higher MMRC scale represented poorer pulmonary function that is also found its association with sarco- 40%; however, this report diagnosed sarcopenia using 22,35 penia in this study. Being underweight increased only low skeletal muscle mass which was defined as the risk of sarcopenia compared to obesity, the results pre-sarcopenia in the current study. These figures support the findings that lower BMI was related to were comparable to the report herein (48 cases, about lower lean mass in COPD patients. BMI was not, 40%). Overall, the prevalence of pre-sarcopenia in however, a good indicator to predict adverse outcome this study is consistent with the previous data that in COPD patients since several studies showed that reported the prevalence of sarcopenia in COPD using only low skeletal muscle mass that varied from 20% BMI was not associated with staging of the disease. 13,31 to 40%. For sarcopenic obesity, the prevalence The explanation was due to the increased extra fat 256 Chronic Respiratory Disease 15(3) stores in greater stages of COPD. Consequently, BMI nonelective admission over the past 12 months, and 14,15 could remain unchanged. Cigarette smoking did BMI status were the factors associated with not show the association with sarcopenia in this study. sarcopenia. The existing reports show inconsistent results. It was one of the related factors in epidemiologic studies. Acknowledgements The mechanism was due to the increased protein cat- The authors would like to acknowledge Professor James A abolism. In contrast, there was evidence that COPD Will, University of Wisconsin–Madison, for editing the patients had a high persistent inflammatory state, with manuscript via Publication Clinic, Khon Kaen University, increased TNF-a which was related to pathophysio- Thailand. logy of sarcopenia, independent of smoking status. Subsequently, cigarette smoking alone did not show 16,36 a significant association with sarcopenia. Sarco- Declaration of conflicting interests penia has been studied as an independent factor for The author(s) declared no potential conflicts of interest decreased bone mineral density (BMD) due to the with respect to the research, authorship, and/or publication systemic consequences of COPD. This study could of this article. not demonstrate this association. One explanation is that prior studies diagnosed sarcopenia using low ske- Funding letal muscle mass alone and analyzed the relationship The author(s) disclosed receipt of the following financial between BMD and sarcopenia, while this study exam- support for the research, authorship, and/or publication of ined the association of the presence of osteoporosis this article: This work was supported by the Neuroscience and sarcopenia. Research and Development Group, Khon Kaen University, There were some limitations of this study. Firstly, Thailand under grant number 001/2558 and the Thailand the overall prevalence of sarcopenia in this study Research Fund (number IRG 5780016). might be under represented as this study estimated gait speed using the 6-MWD. There is evidence that References gait speed taken from the 6-MWD was approxi- mately 17% higher than when the 4-m gait speed 1. Vestbo J, Hurd SS, Agusti AG, et al. Global strategy which was used to measure usual gait speed. 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Sarcopenia in chronic obstructive pulmonary disease: A study of prevalence and associated factors in the Southeast Asian population

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Abstract

Chronic obstructive pulmonary disease (COPD) has been described as a systemic disease. Sarcopenia is one of the systemic effects that is related to several adverse outcomes. The objectives of this study were to estimate the prevalence of sarcopenia and to determine the factors associated with sarcopenia in COPD patients in Southeast Asia. This was a cross-sectional study of COPD patients who attended a COPD clinic from May 2015 to December 2016. Baseline characteristics were collected and dual-energy X-ray absorptiometry was used to measure skeletal muscle mass. Handgrip strength was used to assess muscle strength, and as a measurement of physical performance, the 6-min walk distance was used. One hundred and twenty-one participants were recruited. Most of them were men (92.6%). Prevalence of sarcopenia was 24% (29 cases). Independent factors associated with sarcopenia were age  75 years (adjusted odds ratio (AOR) 13.3, severity of COPD (AOR 19.2 and 13.4 for moderate and severe COPD), Modified Medical Research Council (MMRC) scale (AOD 1.9), and obesity (AOR 0.04). Sarcopenia affects about one-quarter of COPD patients. Age, severity of COPD, MMRC scale, and BMI status were the factors associated with sarcopenia. Keywords Airway obstruction, body composition, fat-free mass index, lung disease, skeletal muscle mass Date received: 27 June 2017; accepted: 20 October 2017 1 Division of Geriatric Medicine, Department of Internal Medicine, Faculty of Medicine,KhonKaenUniversity, Khon Kaen, Thailand Department of Internal Medicine, Faculty of Medicine, Khon Introduction Kaen University, Khon Kaen, Thailand Chronic obstructive pulmonary disease (COPD) is Division of Respiratory System, Department of Internal Medicine, Faculty of Medicine,KhonKaenUniversity, Khon defined as a disease characterized by persistent air- Kaen, Thailand flow limitation that is usually progressive and associ- Division of Nuclear Medicine, Department of Radiology, Faculty ated with an enhanced chronic inflammatory response of Medicine, Khon Kaen University, Khon Kaen, Thailand in the airways and the lung to noxious particles or 5 Division of Ambulatory Medicine, Department of Internal gases. It can lead to substantial morbidity and pre- Medicine, Faculty of Medicine,KhonKaenUniversity, Khon mature death. It affects about 10% of general popula- Kaen, Thailand tion and about 50% of very heavy smokers. Aging is Corresponding author: an independent factor in the prevalence of COPD with Panita Limpawattana, Division of Geriatric Medicine, Department 14% in persons 65 years or over compared with 9.9% of Medicine, Faculty of Medicine, Khon Kaen University, Khon of younger persons. A doubling of the prevalence of Kaen 40002, Thailand. COPD was observed for every 10-year increment in Email: [email protected] Creative Commons CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). Limpawattana et al. 251 age. Existing reports show that COPD is not consi- severity of COPD and BMI is, however, inconsistent 16,17 dered only as a respiratory disease but also described with reports. as a systemic disease including weight loss and nutri- Regarding the current criteria for sarcopenia diag- tional abnormalities, skeletal muscle dysfunction, nosis, they incorporate muscle function which is mus- increased risk of cardiovascular disease, hormonal cle strength and/or physical performance. The and metabolic disturbances, osteoporosis, anxiety, prevalence of sarcopenia in COPD patients according 3–5 and depression. Therefore, a more holistic approach to that definition is limited. Additionally, associated of COPD is essential rather than focusing only on factors of sarcopenia in COPD particularly for the airflow limitations. outcomes involving the geriatric syndrome such as One of the systemic effects of COPD is sarcopenia. falling and disability have not been widely studied. This term has been described as an age-related decline Early detection of sarcopenia could facilitate the 6,7 in muscle mass and its function. This condition is implementation of interventions targeted at prevent- associated with unfavorable health outcomes such as ing the progression of sarcopenia and improving qual- falls, disability, hospitalization, poor quality of life, ity of life in patients with COPD. Therefore, the 8,9 and mortality. The etiology of sarcopenia is the primary objective of this study was to estimate the result of the physiologic changes in addition to the prevalence of sarcopenia in COPD patients and results of disease-related, nutrition, and activity. the secondary objective was to determine the factors Sarcopenia can be classified as physical frailty associated with sarcopenia in COPD patients. where frailty is associated with adverse health out- 11,12 comes. Sarcopenia was found to be associated Material and methods with worsening lung function in male COPD patients. COPD patients also have relative or an Study participants and setting absolute increase in fat mass which might contribute This was a cross-sectional study that was carried out to systemic inflammation, loss of fat-free mass, and with COPD patients who were 18 years old or over insulin resistance. Fat-free mass index, not body mass and attended COPD clinic of Srinagarind Hospital, index (BMI), was significantly related to pulmonary Khon Kaen, Thailand from May 2015 to December function, dyspnea severity, quality of life, and 14,15 2016. This COPD clinic is a tertiary care referral cen- reflected reduced skeletal muscle mass. Cur- ter of the university hospital which enrolled patients rently, the persons with COPD are recommended for from our internal medicine/family medicine clinic sarcopenia screening and assessment according to the and other community hospitals. Patients were recommendation of the Asian Working Group for Sar- 10 excluded if they had other active medical illnesses copenia (AWGS). such as heart failure functional class III–IV, pneumo- The prevalence of sarcopenia in COPD men older nia, septicemia, COPD exacerbation within the pre- than 40 years of age varies from 20% to 40% depend- ceding 4 weeks, patients who were unable to complete ing on age of studied population, gender, setting of 13,16 study due to physical limitations, patients who were population, and measurement methods. The pre- unwilling to participate in this study, and patients who valence of sarcopenia from existing reports in Asia is had limitations in performing dual energy X-ray 29.3% and for sarcopenic obesity is 14.2% ;how- absorptiometry (DXA) or conditions that would affect ever, the definition of sarcopenia from this study DXA results; history of barium taking or enemas over focused only on skeletal muscle mass. In a recent the past 2 weeks, patients who had metallic instru- study in the United Kingdom using the European mentation such as spinal fixation, patients with his- Working Group on Sarcopenia in Older People tory of a radionuclide scan over the past 2 weeks, and (EWGSOP) criteria which included either low mus- patients with a body weight over 200 kg (exceeded the cle strength or poor physical performance with low capacity). The study population was similar to the skeletal muscle mass, it was found at 14.5% among 17 previously published article. stable COPD patients in the outpatient setting. Fac- tors associated with sarcopenia in COPD patients in Definition literature review included age, nutritional status, exercise capacity, severity of COPD, functional per- COPD. COPD was diagnosed in patients according to formance, smoking status, comorbid diseases, and the criteria of the Global Initiative for Chronic Obstruc- self-reported hospital admission. The relation of tive Lung Disease (GOLD) that was characterized by 252 Chronic Respiratory Disease 15(3) persistent airflow limitation, a post-bronchodilator force handgrip strength and 6-MWD was used to measure expiratory volume in 1 s (FEV1) less than 70% of forced physical performance. vital capacity. Severity of COPD was classified into three groups: mild (FEV1>80% normal), moderate (FEV1 50– Procedure 79% normal), and severe (FEV1 <49% normal). For After consent, baseline patient data were collected by patients with severe COPD in this study, it included trained clinical researchers. The demographic infor- patients with severe COPD (FEV1 30–49% normal) and mation consisted of age, sex, educational level, smok- very severe COPD (FEV1 < 30% normal) based on the ing status, severity of COPD using the most recent GOLD staging system. report of pulmonary function tests within the past Sarcopenia. Criteria for sarcopenia diagnosis were 6 months (the patients were asked to take the deepest based on the definition of the AWGS which consists breath they could, and then exhaled into the sensor as of low muscle mass and low muscle strength and/or hard as possible, preferably at least 6 s), MMRC scale, poor physical performance. Skeletal muscle mass was underlying disease, regular medication uses, history estimated using DXA and appendicular skeletal mus- of falls over the past 12 months, self-report baseline cle mass index calculated as appendicular skeletal basic and instrumental activities of daily living (ADL) mass/height (ASMI). Handgrip strength was mea- using Barthel ADLs index and Chula index, history of sured using a handheld dynamometer and measure- nonelective admission over the past 12 months, ment of physical performance that used the 6-min weight, height, and systolic and diastolic blood pres- walk distance (6-MWD) according to the American sure at rest. Weight and height were used to calculate BMI, and systolic and diastolic blood pressures were Thoracic Society guidelines. The following cutoff presented as mean arterial blood pressure (MAP). values were used to identify sarcopenia; ASMI of 2 2 For sarcopenia diagnosis, muscle mass using DXA, 7.0 kg/m for men and 5.4 kg/m for women, and handgrip strength using grip dynamometer (it was either handgrip strength of <26 kg for men and <18 kg measured by asking the patients to hold the handgrip for women or a gait speed of <0.8 m/s. Pre- dynamometer in one hand, with the arm at right sarcopenia is defined as presence of low muscle mass angles and the elbow by the side of the body. When without influence on muscle strength or physical per- ready, the patients squeezed the dynamometer with formance and sarcopenic obesity is characterized by maximum isometric effort, which was maintained for the presence of sarcopenia according to the definition 2 20,21 of the AWGS with BMI > 25kg/m . about 5 s. Three attempts were tested and the maximal one was recorded), and physical performance using Modified Medical Research Council scale. The Modified the 6-MWD as previously described were performed 10,24,25 Medical Research Council (MMRC) scale was used to on all patients in the same period. evaluate dyspnea in daily living. It included five grades (0–4) of various physiological activities that provoke Sample size calculation dyspnea that was self-rated by the patient. The descrip- Sample size calculations were based on the primary tions were as follows: 0, not troubled with breathless- ness except with strenuous exercise; 1, troubled by objective of this study which was the estimated pre- shortness of breath when hurrying on the level or walk- valence of sarcopenia in COPD patients. As there was no study regarding the prevalence of sarcopenia in ing up a slight hill; 2, walked slower than people of the COPD patients according to the definition of the same age on the level because of breathlessness or has to AWGS, the estimated prevalence of 14.5% was stop for breath when walking at own pace on the level; 3, derived from an existing study. The estimation of stopped for breath after walking about 100 yards or after a population proportion with a specified absolute pre- a few minutes on the level; and 4, too breathless to leave cision formula was used to calculate this. At least 98 the house, or breathless when dressing or undressing. participants were sufficient to achieve the required sample size at the significance level of 0.05. Instruments Statistical analyses Muscle mass measurement used DXA (General Elec- tric (Lunar-Progidy) model). A grip dynamometer Descriptive statistics for baseline data were presented (GRIP-D (T.K.K.5401) model) was used to measure in percentage, mean, and standard deviation. If the Limpawattana et al. 253 Table 1. Baseline characteristics of studied population. distribution of these data was not a normal distribu- tion, then medians, and interquartile ranges were used Variables N ¼ 121 instead. Effects of factors associated with sarcopenia were evaluated using univariate and multivariate Age (years), mean (SD) 70 9.0 Age group (years), n (%) regressions analysis. For univariate analysis, crude <65 32 26.45 odds ratios (OR) and 95% confidence intervals (CIs) 65–74 47 38.84 were used to consider the strength of association 75 42 43.71 between factors associated with sarcopenia. Factors Male sex, n (%) 112 92.6 with a p < 0.20 or clinical significance in literature Educational level, n (%) review were then entered into a multiple logistic 6 years or lower 59 48.76 regression model. A value of p < 0.05 was considered 7–12 years 28 23.14 to indicate statistically significant differences, and >12 years 34 28.10 Smoking status, n (%) adjusted OR and their 95% CI were reported to con- Never smoker 7 5.79 sider the strength of association. All the data analyses Ex-smoker 104 85.95 were carried out using STATA version 10.0 (Stata- Current smoker 10 8.26 Corp, College Station, Texas, USA). Severity of COPD, n (%) Ethics approval was provided by the Ethics Com- Mild 31 25.62 mittee of the Faculty of Medicine, Khon Kaen Uni- Moderate 69 57.02 versity as instituted by the Helsinki Declaration. Severe 21 17.36 MMRC scale, mean (SD) 0.69 1.08 Comorbid diseases, n (%) Results Diabetes mellitus 12 9.92 Hypertension 46 38.02 Prevalence of sarcopenia among COPD patients Dyslipidemia 10 8.26 There were 121 participants with stable COPD Chronic arthritis 10 8.26 recruited in this study. Baseline characteristics of the Cancer 6 4.96 studied population are shown in Table 1. The majority Regular medication uses, n (%) Inhaled corticosteroid 113 93.39 of them were men (112 cases, 92.6%) with an age Systemic steroid 2 1.65 older than 65 years old (maximum age was 92 and Oral hypoglycemic drugs 7 5.79 minimum age was 47 years old). Most of them were Statin 13 10.74 ex-smokers with a moderate degree in severity of NSAIDs 1 0.83 COPD. Hypertension was the most common comor- History of fall at least two times over 3 0.89 bid disease. The overall ADL were well-preserved. the past 12 months, n (%) The distribution of low skeletal muscle mass, low Barthel scores, mean (SD) 19.9 1 handgrip strength, and walking speed is demonstrated Chula IADLs scores, mean (SD) 8.98 0.18 Nonelective admission over the past 32 26.45 in Figure 1. Low skeletal muscle mass was the main 12 months, n (%) component, followed by low handgrip strength. Low BMI (kg/m ), n (%) gait speed was found in the minority. According to the Underweight (<18.5) 19 15.7 definition of sarcopenia from the recommendation of Normal and over weight (18.5–24.9) 65 53.72 the AWGS, the prevalence of pre-sarcopenia was Obesity (>25) 37 30.58 about 15.7% (19 cases) and sarcopenia was 24% (29 MAP (mmHg), mean (SD) 95.96 10.68 cases); all of them were men and severe sarcopenia 6-MWD (m), mean (SD) 423.39 73.67 was found in about 2.5% (three cases). The preva- Gait speed (m/s), mean (SD) 1.18 0.2 Handgrip strength (kg), mean (SD) lence of sarcopenic obesity was 0.8% (one case). Male 26.65 6.02 Female 21.22 3.43 Factors associated with sarcopenia among Appendicular skeletal mass index (kg/m ), mean (SD) COPD patients Male 7.1 0.89 Female 6.25 0.46 Comparison of the risk factors between sarcopenic and nonsarcopenic patients with COPD using (continued) 254 Chronic Respiratory Disease 15(3) Table 1. (continued) Table 2. Factors associated with sarcopenia using univari- ate analyses. Variables N ¼ 121 Unadjusted p Osteoporosis, n (%) 45 37.19 Variables OR 95% CI Value Sarcopenia, n (%) 29 24 Age group (years) COPD: chronic obstructive pulmonary disease; NSAIDs: nonster- <65 1 — — oidal anti-inflammatory drugs; IADL: instrumental activities of 65–74 1.2 (0.3, 4.6) 0.8 daily living; BMI: body mass index; MAP: mean arterial blood pres- 75 5.3 (1.6, 17.7) <0.05 sure; SD: standard deviation; osteoporosis: defined when T-score Severity of COPD of femoral neck or lumbar spine 2.5 SD; 6-MWD: 6-min walk Mild 1 — — distance; MMRC scale: Modified Medical Research Council scale Moderate 3.3 (0.9, 12.2) 0.07 (it was available in 116 patients). Appendicular skeletal mass was calculated by summing the mus- Severe 5.7 (1.3, 25.3) <0.05 cle masses of the four limbs. MMRC scale 1.9 (1.3, 2.8) <0.05 Comorbid diseases Diabetes mellitus 1.1 (0.3, 4.2) 0.9 Hypertension 1.2 (0.5, 2.8) 0.7 Dyslipidemia 0.8 (0.2, 3.9) 0.8 Chronic arthritis 1 (omitted) Cancer 1.6 (0.3, 9.4) 0.6 Regular medication uses Inhaled corticosteroid 0.9 (0.2, 4.9) 0.9 Systemic steroid 3.3 (0.2, 53.7) 0.4 Oral hypoglycemic drugs 0.5 (0.1, 4.4) 0.5 Statin 1.5 (0.4, 5.2) 0.6 NSAIDs 1 (omitted) History of falls at least 1.6 (0.1, 18.4) 0.7 2 times over the past 12 months Barthel scores 1 (omitted) Chula IADLs scores 1 (omitted) Nonelective admission 2.0 (1.1, 3.7) <0.05 over the past 12 months BMI (kg/m ) Underweight 1 Figure 1. The relationship of low skeletal muscle mass, Normal and over weight 0.3 (0.1, 0.8) <0.05 Obesity 0.02 (002, 0.2) <0.05 low handgrip strength, and low gait speed in study populations. MAP (mmHg) 0.9 (0.9, 0.9) <0.05 Osteoporosis 1.8 (0.8, 4.3) 0.2 univariate analysis is shown in Table 2. For multivariate COPD: chronic obstructive pulmonary disease; OR: odds ratio; analysis, six factors where p < 0.2 or clinical signifi- CI: confidence interval; BMI: body mass index; MAP: mean arterial blood pressure; osteoporosis: defined when T-score of femoral cance from literature review from univariate analysis neck or lumbar spine 2.5 standard deviation; MMRC scale: were entered in the multiple regression models: age, Modified Medical Research Council scale; NSAIDs: nonsteroidal severity of COPD, MMRC scale, nonelective admission anti-inflammatory drugs; IADL: instrumental activities of daily over the past 12 months, BMI, MPA, and presence of living. osteoporosis (Table 3). After multicollinearity was checked, advanced age (>75 years), greater severity of prevalence of sarcopenia was about 1 in four of COPD, MMRC scale, and nonobese patients were the factors associated with sarcopenia in this study. all COPD patients. This finding was higher than pre- viously reported in the United Kingdom which was 14.5% but was comparable to the study in South 17,27 Discussion Korea which reported 25%. The possible expla- nations are the differences in body composition of This is the first study that examines sarcopenia in different ethnicities and Asian people appear to COPD using AWGS criteria in Southeast Asia. The Limpawattana et al. 255 Table 3. Factors associated with sarcopenia using multi- was very low in this study (0.8%). To the best of variate analyses. authors’ knowledge, there has been no study using similar criteria in COPD patients. The prevalence of Adjusted sarcopenic obesity in Asia in existing studies is about Variables OR 95% CI p Value 15%; however, this current study used only skeletal 13,32 Age group (years) muscle mass to detect sarcopenia. <65 1 — — There were four factors associated with sarcopenia 65–74 2.0 (0.4, 10.8) 0.4 using multivariate analyses: age, severity of COPD, 75 13.3 (2.2, 79.9) <0.05 MMRC scale, and BMI. Advancing age and severity Severity of COPD of COPD showed high magnitudes of associations. Mild 1 — — Commonly, a progressive loss of muscle mass occurs Moderate 19.2 (2.2, 166.4) <0.05 Severe 13.4 (1.2, 148.6) <0.05 at the age of 40 and is greater after 70 years. The MMRC scale 1.9 (1.1, 3.3) <0.05 decline in gait speed and grip strength was faster than 21,33 Nonelective admission 3.3 (0.8, 12.9) 0.1 muscle mass especially after the age of 70 years. over the past The result supports that age is one of the independent 12 months factors; however, only age >75 years showed statisti- BMI (kg/m ) cal significance. Because the patients in this study Underweight 1 — — were with age over than 40 years old, an age of Normal and over 1.6 (0.3, 7.9) 0.6 weight 65–74 years compared to an age of less than 65 years Obesity 0.04 (0.003, 0.6) <0.05 might not show the differences. For the severity of MAP (mmHg) 0.9 (0.9, 1.0) 0.1 COPD, it was consistent with the previous reports that Osteoporosis 1.4 (0.4, 5.1) 0.6 skeletal muscle masses were lower in a greater degree 14,17 of airflow limitation. This association might be COPD: chronic obstructive pulmonary disease; OR: odds ratio; CI: confidence interval; BMI: body mass index; MAP: mean arterial explained by (1) high resting energy expenditure as a blood pressure; osteoporosis: defined when T-score of femoral result of increased work of breathing and inadequate neck or lumbar spine 2.5 standard deviation; MMRC scale: dietary intake in severe COPD, (2) physical inactivity Modified Medical Research Council scale. due to exercise intolerance, (3) excessive apoptosis of skeletal muscle due to increased systemic inflamma- have a higher prevalence of sarcopenia than other tion, and (4) possible presence of hypoxia and the regions. Additionally, the variation of techniques more frequent use of systemic corticosteroids. Con- to estimate all parameters to diagnose sarcopenia is versely, severity of COPD showed no association with another reason. The study in the United Kingdom some reports; this might be due to the definition of diagnosed COPD using EWGSOP criteria and mea- sarcopenia that used low skeletal muscle mass alone sured skeletal muscle mass with bioelectrical impe- in that study while muscle strength and physical per- dance analysis (BIA) and quadriceps strength to formance were additional factors associated with evaluate muscle strength, whereas this study used severity of COPD did not measure. The MMRC DXA to measure skeletal muscle mass and handgrip scale increased the risk of sarcopenia. This finding 17,27 strength to rate muscle strength. Although BIA pre- was similar to the prior report. This scale had sents good reliability and correlation to DXA, BIA been widely studied regarding its correlation with underestimated muscle mass compared to DXA in pulmonary function tests. Additionally, it could pre- 29,30 22,35 prior studies. The study in Brazil regarding the dict morbidity and mortality in COPD patients. prevalence of sarcopenia in COPD using DXA was Higher MMRC scale represented poorer pulmonary function that is also found its association with sarco- 40%; however, this report diagnosed sarcopenia using 22,35 penia in this study. Being underweight increased only low skeletal muscle mass which was defined as the risk of sarcopenia compared to obesity, the results pre-sarcopenia in the current study. These figures support the findings that lower BMI was related to were comparable to the report herein (48 cases, about lower lean mass in COPD patients. BMI was not, 40%). Overall, the prevalence of pre-sarcopenia in however, a good indicator to predict adverse outcome this study is consistent with the previous data that in COPD patients since several studies showed that reported the prevalence of sarcopenia in COPD using only low skeletal muscle mass that varied from 20% BMI was not associated with staging of the disease. 13,31 to 40%. For sarcopenic obesity, the prevalence The explanation was due to the increased extra fat 256 Chronic Respiratory Disease 15(3) stores in greater stages of COPD. Consequently, BMI nonelective admission over the past 12 months, and 14,15 could remain unchanged. Cigarette smoking did BMI status were the factors associated with not show the association with sarcopenia in this study. sarcopenia. The existing reports show inconsistent results. It was one of the related factors in epidemiologic studies. Acknowledgements The mechanism was due to the increased protein cat- The authors would like to acknowledge Professor James A abolism. In contrast, there was evidence that COPD Will, University of Wisconsin–Madison, for editing the patients had a high persistent inflammatory state, with manuscript via Publication Clinic, Khon Kaen University, increased TNF-a which was related to pathophysio- Thailand. logy of sarcopenia, independent of smoking status. Subsequently, cigarette smoking alone did not show 16,36 a significant association with sarcopenia. Sarco- Declaration of conflicting interests penia has been studied as an independent factor for The author(s) declared no potential conflicts of interest decreased bone mineral density (BMD) due to the with respect to the research, authorship, and/or publication systemic consequences of COPD. This study could of this article. not demonstrate this association. One explanation is that prior studies diagnosed sarcopenia using low ske- Funding letal muscle mass alone and analyzed the relationship The author(s) disclosed receipt of the following financial between BMD and sarcopenia, while this study exam- support for the research, authorship, and/or publication of ined the association of the presence of osteoporosis this article: This work was supported by the Neuroscience and sarcopenia. Research and Development Group, Khon Kaen University, There were some limitations of this study. Firstly, Thailand under grant number 001/2558 and the Thailand the overall prevalence of sarcopenia in this study Research Fund (number IRG 5780016). might be under represented as this study estimated gait speed using the 6-MWD. There is evidence that References gait speed taken from the 6-MWD was approxi- mately 17% higher than when the 4-m gait speed 1. Vestbo J, Hurd SS, Agusti AG, et al. Global strategy which was used to measure usual gait speed. 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Chronic Respiratory Disease – Pubmed Central

Published: Nov 29, 2017

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