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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 11  |  Issue : 2  |  Page : 162-168

Pulmonary Rehabilitation Reduces the Sarcopenia Phenotype in Patients with Chronic Obstructive Pulmonary Disease


1 Department of Basic Medical Sciences, College of Medicine, University of Sharjah, Sharjah, United Arab Emirates, United Arab Emirates
2 Department of Biochemistry, Gomal Medical College, Gomal University, Dera Ismail Khan, Pakistan

Date of Submission23-Jan-2022
Date of Decision21-Feb-2022
Date of Acceptance21-Feb-2022
Date of Web Publication08-Apr-2022

Correspondence Address:
Dr. Rizwan Qaisar
Department of Basic Medical Sciences, College of Medicine, University of Sharjah, Sharjah
United Arab Emirates
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijrc.ijrc_20_22

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  Abstract 


Purpose: Sarcopenia or age-associated muscle decline is common in patients with chronic obstructive pulmonary disease (COPD). Pulmonary rehabilitation (PR) is an effective tool in reducing COPD phenotype, but its effects on sarcopenia and functional capacity are poorly known. We aimed to assess the restorative potential of PR on skeletal muscle and physical capacity in COPD patients. Methods: We investigated the male COPD patients, 56–71 years old (n = 55), through clinical examination, laboratory investigation, and spirometry. All patients were evaluated at two time points, 1 year apart before and following the PR. Reduced handgrip strength (HGS), appendicular skeletal mass index (ASMI), and gait speed were considered the clinical indexes of Sarcopenia. Enzyme-linked immunosorbent assay were used to measure the circulating markers of inflammation (C-reactive protein [CRP]) and oxidative stress (8-isoprostanes). Results: At baseline, the COPD patients had low HGS and gait speed and elevated CRP and 8-isoprostanes levels. According to four internationally recognized criteria, these patients also had a high incidence of Sarcopenia. One year of PR partially restored the HGS, gait speed, CRP, and 8-isoprostanes levels (all P < 0.05). However, the ASMI values were insignificantly restored following PR. PR also reduced the incidence of sarcopenia in COPD patients. Among various criteria for sarcopenia, the international working group on sarcopenia yielded the highest incidence of sarcopenia in COPD patients. Conclusion: Altogether, our data show the therapeutic potential of PR in skeletal muscle, physical performance, and systemic health in patients with COPD.

Keywords: 8-isoprostanes, chronic obstructive pulmonary disease, C-reactive protein, handgrip strength, pulmonary rehabilitation, sarcopenia


How to cite this article:
Altamimi A, Shuaeeb A, Yakout A, Hassouna D, Srouji H, AlQaydi M, Mahmoud MM, Alkindi N, Kashmoola Q, Alkhatib R, Soudan R, Tawileh RA, Muhammad T, Qaisar R. Pulmonary Rehabilitation Reduces the Sarcopenia Phenotype in Patients with Chronic Obstructive Pulmonary Disease. Indian J Respir Care 2022;11:162-8

How to cite this URL:
Altamimi A, Shuaeeb A, Yakout A, Hassouna D, Srouji H, AlQaydi M, Mahmoud MM, Alkindi N, Kashmoola Q, Alkhatib R, Soudan R, Tawileh RA, Muhammad T, Qaisar R. Pulmonary Rehabilitation Reduces the Sarcopenia Phenotype in Patients with Chronic Obstructive Pulmonary Disease. Indian J Respir Care [serial online] 2022 [cited 2022 Jun 29];11:162-8. Available from: http://www.ijrc.in/text.asp?2022/11/2/162/342773




  Introduction Top


Sarcopenia or age-associated muscle detriment contributes to frailty and functional impairment in the elderly,[1] with a risk of reduced quality of life and premature death.[2] The evaluation of sarcopenia includes the assessments of muscle strength and mass and physical performance.[3] Low handgrip strength (HGS) is a powerful marker of muscle weakness and reduced quality of life in aging.[4] The decline in HGS may be a powerful marker of sarcopenia and several age-associated pathologies.[5],[6] Low appendicular skeletal mass index (ASMI) indicates muscle wasting and physical dependency.[7] Walking speed is a measure of physical capacity, as people with low walking speed have poor health.[8]

Several age-related diseases worsen the sarcopenia phenotype. Chronic obstructive pulmonary disease (COPD) is a well-characterized disease in the elderly.[9] COPD is primarily a lung disease with systemic consequences, including skeletal muscle detriment. Approximately 30%–40% of COPD patients experience muscle atrophy and weakness, which can further compromise the physical independence of these patients.[10]

Muscle atrophy is frequently associated with muscle weakness and can compromise physical independence.[10] COPD patients with muscle wasting and weakness are mostly bedridden or sedentary, which further compromises their lung function and worsens the COPD.[11] Consequently, a weaker muscle in COPD patients may indicate advanced disease and poor survival. Thus, restoring muscle mass and strength may be an attractive treatment strategy in COPD.

Regular exercises are an effective protective strategy for sarcopenia in COPD patients[12] since increased muscle force and functional performance are reported in most exercise trials.[13] Endurance exercise appears to be a helpful intervention to prevent muscle loss and may be more effective in combination with resistance exercise.[14] Pulmonary rehabilitation (PR) is a useful intervention to restore physical capacity and skeletal muscle in COPD.[15] PR is a composite program and involves endurance exercises,[16] in addition to counseling sessions. Several studies indicate that PR can effectively reduce lung and skeletal muscle impairment in COPD.[16] In addition, since skeletal muscle plasticity is reduced in COPD, it is essential to implement PR over a long period. Therefore, the studies implementing PR over shorter periods may not fully encompass COPD's muscle and lung recovery.

Several studies appreciate the roles of PR in positively modulating the exercise capacity of COPD patients in addition to improved arterial oxygenation,[17] health-related quality of life,[18] and body composition[19] over short periods over weeks to months. However, the long-term effects of PR on sarcopenia phenotype in COPD are poorly known. They require a thorough characterization of muscle and systemic health to understand the exercise efficacy better.

We investigated the effects of PR on sarcopenia phenotype, physical capacity, and generalized health in patients with COPD over 1 year. We hypothesize that PR can help reduce the sarcopenia phenotype in COPD patients. We aim to address this hypothesis by investigating COPD patients during PR.


  Methods Top


Study design and participants

We recruited COPD patients after gaining approval from the regional ethical committee at the teaching hospitals (anonymized for blinded review). All patients (n = 55) were males aged 56–71 years and provided written informed consent for clinical assessment, laboratory investigation, and spirometry analysis. All measurements were taken at two visits, 1 year apart. After baseline recordings at visit-1, the COPD patients were placed on PR therapy, a composite program that includes aerobic exercises, counseling, and psychological support with at least three sessions of 2–4 h per week [Table 1]. The exercise program had brisk walking, a treadmill, or a stationary bicycle for ≥30 min to achieve 60%–80% of the peak work rate.[16] The walking speed as a measure of a 4-meter walking test (m/s) and steps count (steps/d) was assessed at baseline and following the conclusion of PR.
Table 1: The primary components of the pulmonary rehabilitation program in this study

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All participants were randomly selected from an existing cohort to avoid selection bias.[6],[9],[20] COPD was defined as postbronchodilator forced expiratory volume (FEV1)/forced vital capacity (FVC) ratio <0.70 with continuing respiratory symptoms, according to the GOLD guidelines.[21] Participants with a steady and stable condition were included, while others with unstable conditions (infection and/or hospitalization in the previous month), myopathies, neurological diseases, and related comorbidities were excluded.

Handgrip strength measurement

HGS was measured with a digital handgrip dynamometer (CAMRY, South El Monte, CA, USA), as described before.[22] The participants were seated in a supine position with their elbows flexed at a 90° angle and then instructed to squeeze the dynamometer as hard as they could without jerking or wrenching. During the process, no other movement was permitted. Three tries were made with each hand, with a 60-s rest in between, and the highest measurement was recorded for analysis, as previously mentioned.[9] The body mass index (BMI) was reported as Kg/m2. Bioelectrical impedance was used to determine the appendicular skeletal muscle mass (ASM), which was normalized to height in square meters to obtain the appendicular skeletal mass index (ASMI).[20]

Spirometry

The FEV1 and FVC were measured using a portable spirometer (Contec SP10, Qinhuangdao, Hebei, China). Quality-control processes were implemented, and technicians set spirometers according to the American Thoracic Society/European Respiratory Society repeatability standards, before conducting spirometry early morning.[23]

Measurements of plasma 8-isoprostanes and C-reactive proteins

We used the enzyme-linked immunosorbent assay to measure 8-isoprostanes (Cayman Chemical, Ann Arbor, MI, USA) and C-reactive protein (CRP) (R and D Systems, Minneapolis, MN, USA) levels in the blood samples collected early morning in the fasting state, as described previously.[9]

Statistical analysis

The data matched the assumption of normality using a Chi-square normality test. The anthropometric measurements of the subjects were presented using mean and standard deviation.[13] The Chi-square test was implied to determine categorical variables between the groups. The strength of relation of sarcopenia indexes with plasma biomarkers was evaluated using Pearson correlation. Sarcopenia incidence was compared according to various criteria with a two-sample t-test. P < 0.05 was statistically significant. GraphPadPrism (Graph Pad Software, San Diego, California, CA, USA) version 8.0.2 was used for all statistical analyses.


  Results Top


Body composition, spirometry performance, and plasma biochemistry

The basic characteristics of COPD patients are described in [Table 2]. Overall, there was no difference in the COPD patients' BMI, ASM, fat mass, and plasma chemistry profile between the two visits. Conversely, PR resulted in an improvement in phase angle, FEV1, and FEV1 (predicted) in COPD patients (all P < 0.05) [Table 2].
Table 2: Demography and primary characteristics of the participants

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Indexes of sarcopenia and physical capacity

At baseline, HGS in COPD patients was 24.08 ± 3.83 kg, restored to 26.95 kg following PR (P = 0.009) [Figure 1]a.
Figure 1: The indexes of Sarcopenia and physical capacity in chronic obstructive pulmonary disease patients before (visit 1) and following (visit 2) 1 year of pulmonary rehabilitation. Chronic obstructive pulmonary disease was associated with reduced handgrip strength (a), unaltered appendicular skeletal mass index (b), lower 4-meter walking test, gait speed (c), and an unchanged daily step count (d). One year of pulmonary rehabilitation incompletely restored the handgrip strength and 4-meter walking test in chronic obstructive pulmonary disease patients. All values are represented as mean ± standard deviation, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001

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Since HGS is influenced by muscle mass, we next measured the ASMI as an indicator of muscle mass. However, PR did not change the ASMI in COPD patients [Figure 1]b. Next, we measure walking speed as an indicator of functional capacity. PR significantly increased the walking speed in COPD patients compared to the baseline values (1.01 ± 0.30 m/s vs. 0.81 ± 0.14 m/s) [Figure 1]c. Daily step count is a useful and cost-effective measure of physical activity. PR resulted in a trend toward an increase in step count in COPD patients than baseline values (3475 ± 831 vs. 3231 ± 517 steps/day) [Figure 1]d. However, the difference failed to reach statistical significance.

Blood C-reactive protein and 8-isoprospanes levels

Since systemic inflammation contributes to sarcopenia phenotype, we next measured the CRP levels in the blood as a marker of inflammation. COPD patients at baseline had blood CRP levels of2.98 ± 0.39 mg/dl. PR significantly reduced the plasma CRP levels to 2.67 mg/dl (P < 0.0001) [Figure 2]a. Since elevated oxidative stress can also drive sarcopenia, we next measured blood 8-isoprostanes levels in COPD patients during PR. COPD patients had blood 8-isoprostanes levels of111.61 ± 21.79 pg/ml at baseline. Following the PR, blood 8-isoprostanes levels dropped to85.35 ± 19.97 pg/ml, which were significantly lower than the baseline levels (P < 0.0001) [Figure 2]b.
Figure 2: Levels of blood C-reactive protein (a) and 8-isoprostanes (b) in chronic obstructive pulmonary disease patients before (visit 1) and after (visit 2) following one year of pulmonary rehabilitation. C-reactive protein C-reactive protein and 8-isoprostanes were higher in chronic obstructive pulmonary disease patients at baseline and were partly reduced with pulmonary rehabilitation. All values are represented as mean ± standard deviation. **** P ≤ 0.0001

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Effects of pulmonary rehabilitation on indexes of sarcopenia and physical activity using paired-wise comparisons

We next conducted paired t-tests on COPD patients to track the PR induced-alterations in sarcopenia indexes in individual patients over 1 year period. PR significantly improved the HGS in COPD patients over a year (11.93% increase, P = 0.0009) [Figure 3]a. Among the individual patients, 38 patients showed an increase in HGS, while 17 patients did not increase HGS following PR. On the other hand, ASMI was not altered following PR in COPD patients [Figure 3]b. To determine the potential improvement in physical activity of COPD patients, we next observed how PR affected walking speed and step count in COPD patients. Walking speed increased significantly after PR (24% improvement, P < 0.0001), as an increase was reported in 39 out of 55 patients [Figure 3]c.
Figure 3: Paired-wise comparisons showing the effect of 1 year of pulmonary rehabilitation on indexes of Sarcopenia and the physical activity in chronic obstructive pulmonary disease patients. Pulmonary rehabilitation significantly increased handgrip strength (a) and 4-meter walking speed (c) in chronic obstructive pulmonary disease patients, without altering appendicular skeletal mass index (b) and daily steps count (d). Pulmonary rehabilitation also reduced the plasma C-reactive protein (e) and 8-isoprostanes (f) levels in chronic obstructive pulmonary disease patients

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On the other hand, we did not find any increase in daily step count following PR in COPD patients [Figure 3]d. We next investigated the effects of PR on plasma CRP in COPD patients. PR significantly reduced the CRP levels in COPD patients when compared to baseline (10.3% reduction, P < 0.0001), as 42 out of 55 patients reported a decrease in CRP following PR [Figure 3]e. Finally, we measured blood 8-isoprostanes levels in COPD patients and found that PR decreased the 8-isoprostane levels in the blood (23.5% reduction, P < 0.0001) [Figure 3]f. In the COPD cohort, 46 patients reported a decline, while nine patients did not report a decrease in plasma 8-isoprostane levels following PR.

Incidence of sarcopenia

We investigated the sarcopenia incidence based on different criteria in COPD patients. Sarcopenia incidence was higher at baseline than following PR irrespective of the criteria applied [Figure 4]. PR significantly reduced the sarcopenia incidence in COPD patients regardless of the criteria applied. A comparison among sarcopenia criteria revealed that the criteria adopted by the International Working Group on Sarcopenia (IWGS) yielded the highest incidence of sarcopenia in COPD patients independent of the PR status [Figure 4].
Figure 4: Sarcopenia incidence in chronic obstructive pulmonary disease patients before (visit 1) and following (visit 2) one year of pulmonary rehabilitation, based on four internationally recognized diagnostic criteria of Sarcopenia. Asian Working Group for Sarcopenia; European Working Group on Sarcopenia in Older People; Foundation for the National Institutes of Health; International Working Group on Sarcopenia. Values are represented as percentages, *P < 0.05, ** P < 0.01, ***P < 0.001

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The incidence of sarcopenia according to EWGSOP and Asian Working Group on Sarcopenia (AWGS) criteria was 21.82% in the COPD patients before PR, which was reduced to 7.27% following the PR. The criteria by the IWGS yielded the highest incidence of sarcopenia before (56.36%) and following (30.91%) PR [Figure 4]. The Foundation for National Institute of Health (FNIH) criteria, which considers HGS and gait speed as parameters of sarcopenia, showed the most substantial drop in Sarcopenia following the PR. At the first visit, 40% of COPD patients were diagnosed with sarcopenic, but at the second visit, the figure had significantly dropped to 9.09% (P < 0.001) [Figure 4].


  Discussion Top


We investigated the efficacy of PR in preventing or reducing sarcopenia phenotype in COPD patients. Following PR, a significant improvement in HGS and walking speed was found, indicating improved muscle quality and functional capacity. These changes were accompanied by a reduction in plasma CRP and 8-isoprostanes, indicating reduced systemic inflammation and oxidative stress. However, PR had no effect on ASMI and daily step count.

PR is a useful measure to improve the health status of COPD patients. This study showed an improvement in the physical capacity of COPD patients following PR. These findings support a previous report showing a sarcopenia prevalence of 15% in COPD patients. These patients had lower exercise and functional capacity, BMI, and muscle weakness. PR improved their physical capacity and reversed sarcopenia in 12 out of 43 patients.[24] Moreover, according to other studies, PR improves exertional dyspnea, breathing pattern, and dynamic hyperinflation. Lan et al. also reported that general training strengthened the respiratory muscles, which aids in the reduction of dyspnea.[25]

COPD patients had elevated blood CRP and 8-isoprostanes at baseline, partially restored to normal levels following PR. Skeletal muscle atrophy seen in COPD patients is related to systemic inflammation, while higher-than-normal levels of CRP are related to reduced physical capacity and abnormal energy metabolism.[26] The decrease in physical capacity is a predictor of a poorer prognosis and is attributed to muscle atrophy, in addition to impaired cardiac output and tissue hypoxia.[10],[26] Although limited by small sample size, some data show reduced muscle regenerative capacity in patients with COPD.[27] Therefore, COPD negatively affects skeletal muscles and increases the risk of sarcopenia.

We implemented a PR program consisting of endurance training, education, and psychological support as 2–4-h sessions done 3 times per week. The exercises program included regular exercises of high intensity for at least 30 min on the treadmill or stationary bicycle or as walks, intending to reach 60%–80% of the patient's peak work rate. Consistent with our data, a previous study found that aerobic exercises promote muscle health in COPD patients, including improved walking speed, chair rise time, functional performance, fatigue scores, and quality of life.[28] In addition, high-intensity training benefits increasing oxygen uptake and peripheral muscle and cardiovascular function.[25] A recent meta-analysis reported that a minimal PR program of 4 to 12 weeks included lower limb endurance exercises, dyspnea, exercise capacity and performance, and health-related quality of life without improving the daily physical activity.[29] This current study involves high-intensity endurance training as part of a PR program that improved HGS and exercise capacity and reduced inflammation, with positive effects on the health status of patients. Further, outcomes such as improved lung function and reduced sarcopenia phenotype make PR an attractive therapeutic strategy in COPD patients.[24]

In this study, we used the plasma CRP as a marker for inflammation and isoprostanes as a marker of oxidative stress in COPD patients. We show that CRP levels and blood 8-isoprostane levels were significantly reduced after PR, indicating mitigation of generalized inflammation and oxidative stress, which can be helpful for the clinical management of COPD.[30]

The diagnostic criteria of sarcopenia caries across academic societies such as EWGSOP, IWGS, AWGS, and FNIH.[31] Moreover, different definitions may change the diagnosis of sarcopenia, resulting in variations in disease prevalence.[32] The EWGSOP2 criteria that we used for the diagnosis of sarcopenia define it as a reduction in muscle mass (ASMI <7.0 kg/m2 for males and <5.5 kg/m2 for females), HGS (<27 kg for males and <16 kg for females), and gait speed (≤0.8 m/s both for males and females), which are associated with poor quality of life, physical disability, and high mortality.[33] On the other hand, FNIH criteria define sarcopenia as low HGS (<26 kg for males and <16 kg for females) and low muscle mass (ASM adjusted for BMI <0.789 for men and <0.512 for women).[34] There is, however, a low degree of agreement between FNIH and EWGSOP2 definitions, so the two cannot be used interchangeably.[35] A study by Bianchi et al. indicated that the EWGSOP2 criteria had the best predictive value for mortality.[35] Our data are consistent with these findings indicating different incidences of sarcopenia when each criterion was individually applied. Among different criteria, EWGSOP may be more clinically relevant since it considers muscle strength, mass, and walking speed as composite measures of daily physical activity.

This study has some limitations. First, we measured the muscle strength of the upper extremities only. However, the strength of lower extremities may be more relevant to sarcopenia due to its stronger association with a dependent lifestyle.[36] However, other studies have shown a comparable decline in upper and lower extremities strength with aging,[37] boosting our confidence in HGS as an indicator of generalized muscle decline. In addition, we cannot rule out the potential contributions of altered nutrition and hormonal levels among subjects, as these factors can independently influence muscle mass and strength. However, we are confident that nutritional and hormonal variations across subjects are minimal due to our study population's comparable BMI, genetics, socioeconomics, and cultural factors. Our study only includes male subjects, so our findings may not completely apply to females. Large sample size may be required to draw more definite conclusions in future studies. Further research should include women and men of diverse genetic backgrounds and a larger sample size. It will also be worth considering adding more parameters in the analysis, such as nutritional or hormonal factors, to better understand what other factors contribute to a reduction in muscle mass.


  Conclusions Top


Altogether, we show that COPD is associated with exacerbated sarcopenia phenotype, resulting in disabilities and decreased quality of life. However, PR can effectively restore physical capacity and skeletal muscle strength in COPD patients. At molecular levels, PR reduces blood CRP and 8-isoprostanes levels, indicating reduced generalized inflammation and oxidative stress. Our findings indicate PR as an effective therapeutic strategy to restore skeletal muscle and functional health in COPD.

Financial support and sponsorship

This work was financially supported by Target (1901090168) and competitive grants (2001090177) from the University of Sharjah to Rizwan Qaisar.

Conflicts of interest

There are no conflicts of interest.



 
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