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ORIGINAL ARTICLE
Year : 2019  |  Volume : 36  |  Issue : 3  |  Page : 188-192  

Exacerbation of chronic obstructive pulmonary diseases as a risk factor of the skeletal muscle dysfunction


Department of Propedeutics of Internal Medicine, National Pirogov Memorial Medical University, Vinnytsya, Ukraine

Date of Web Publication24-Apr-2019

Correspondence Address:
Dr. Vitalii Poberezhets
Department of Propedeutics of Internal Medicine, National Pirogov Memorial Medical University, Vinnytsya, Khmelnytsky Highway 96
Ukraine
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/lungindia.lungindia_185_18

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   Abstract 


Background: Exacerbation of Chronic Obstructive Pulmonary Disease (COPD) contributes to increased systemic inflammation, oxidative stress, hypoxia, hypercapnia and other risk factors of the skeletal muscle dysfunction. Aims and Objectives: This study aimed to determine whether the frequency of the COPD exacerbations promotes deterioration of the skeletal muscle dysfunction in patients with COPD and to figure out which characteristics of the muscles will reflect this changes. Materials and Methods: We examined 98 male COPD patients, mean age 60.4±11.2 years, GOLD groups B, C, D. To assess the degree of skeletal muscle dysfunction we used hand-grip strength, 6-minute walk test, bioelectrical impedance analysis. Quality of life was evaluated using St. George's respiratory questionnaire (SGRQ). Results: Increase in the frequency of COPD exacerbations was associated with the decrease in the 6-minute walk test distance (r= -0.214, P = 0.034) and with the rise of sarcopenia according to the results of bioelectrical impedance analysis – lower fat-free mass index (r = -0.201, P = 0.047). Frequency of COPD exacerbations had a weak correlation with the degree of the activity limitation component of SGRQ (r = 0.436, P < 0.001). Conclusions: COPD exacerbation plays an important role in progression of the skeletal muscle dysfunction. It decreases endurance of the skeletal muscles, diminishing their size, which manifests itself in reduced exercise tolerance. Increase in the frequency of the COPD exacerbations also worsens all components of the life quality.

Keywords: Chronic obstructive pulmonary disease exacerbation, comorbidity, skeletal muscle dysfunction


How to cite this article:
Poberezhets V, Mostovoy Y, Demchuk H. Exacerbation of chronic obstructive pulmonary diseases as a risk factor of the skeletal muscle dysfunction. Lung India 2019;36:188-92

How to cite this URL:
Poberezhets V, Mostovoy Y, Demchuk H. Exacerbation of chronic obstructive pulmonary diseases as a risk factor of the skeletal muscle dysfunction. Lung India [serial online] 2019 [cited 2019 Jul 21];36:188-92. Available from: http://www.lungindia.com/text.asp?2019/36/3/188/256917




   Introduction Top


Skeletal muscles dysfunction is chronic obstructive pulmonary disease (COPD) comorbidity, which significantly affects the quality of life, functional state of the organism, and surviving of the patients.[1] Development of the skeletal muscle dysfunction in COPD patients contributes to the presence of numerous risk factors, which include reduced physical activity during the day,[2] smoking,[3] hypoxia,[4] hypercapnia,[5] oxidative stress,[6] usage of the systemic glucocorticosteroids,[7] malnutrition,[8] systemic inflammation,[9] imbalance of anabolic and catabolic hormones,[10] and Vitamin D insufficiency.[11]

COPD exacerbation is an acute condition, which is extremely important for patients, increasing frequency of hospitalization, worsening life quality, and ventilatory function.[12] In addition to this negative effect on the progression of COPD, exacerbation indirectly through the action of various catabolic stimuli promotes the progression of skeletal muscle dysfunction. Patient's organism during exacerbation is intensively affected by the following risk factors of the skeletal muscle dysfunction: hypoxia,[13] hypercapnia,[14] malnutrition,[15] decreased physical activity,[16] increased systemic inflammation,[17] administration of the systemic glucocorticosteroids,[7] oxidative stress,[18] and decrease in the level of anabolic hormones.[10]

In this study, we used the handgrip dynamometry, bioelectrical impedance analysis, and 6-min walking test (6MWT) in stable COPD patients and compared it with COPD exacerbation frequency to assess the influence on skeletal muscles.


   Materials and Methods Top


This was a prospective cross-sectional study carried out in the Propedeutic Department to Internal Medicine, National Pirogov Memorial Medical University, Vinnytsia, and Pulmonological Department of the Vinnitsia City Clinical Hospital No 1, Vinnytsia, Ukraine.

We examined the patients discharged from the pulmonology department after treatment of COPD exacerbation. The study was conducted after being approved by the Ethical Committee of the University and obtaining informed consent from the patients.

We examined 98 male patients with stable COPD, mean age – 60.4 ± 11.2 years. Demographic and clinical characteristics of patients are presented in [Table 1].
Table 1: Demographic and clinical characteristics of the patients

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COPD was diagnosed on the basis of past history, physical examination, and spirometric data according to the Global Initiative for Obstructive Lung Disease guidelines.[19]

Patients belonged to the COPD groups B, C, and D. The distribution of these groups was as follows: Group B – 31 patients (31.6%), Group C – 42 patients (42.9%), and Group D – 25 patients (25.5%). All patients received a standard therapy according to the COPD group to which they belong.

We use a specific program for patient history monitoring in Vinnytsia region – “Doctor Eleks” assessed the history of previous COPD exacerbations. We assessed the frequency of exacerbation, obtained treatment, and evidence of hospitalization.

Assessment of the skeletal muscle dysfunction (SMD) was done by studying the functional state of skeletal muscles (strength, endurance) and its mass. Skeletal muscles strength was estimated using handgrip dynamometry of the dominant hand with a certified handgrip dynamometer “DK-100” with further comparison of the obtained data with the age normal values for this gender.[20] The method provided a three-time measurement by maximal isometric handgrip muscle contraction with the registration of the best attempt.

Endurance, needed for evaluation of exercise tolerance, was determined by the 6MWT.[21] During this test, we assessed distance walked for 6 min, number of stops, use of the short-acting bronchodilator, and degree of shortness of breath at the beginning and at the end of the test by Borg Scale.

Bioelectrical impedance analysis was used to investigate skeletal muscle mass. This method is recommended for assessing the skeletal muscle mass in patients with COPD by the European Working Group on Sarcopenia in Older People[22] and was chosen by us because of its mobility, speed in usage, and low cost. Using bioelectrical impedance, we obtained skeletal muscle percentage in the body and fat-free mass (FFM). Other more sensitive indicators for assessment skeletal muscle mass were calculated based on it: FFM Index (FFMI) and Skeletal Muscle Index (SMI). FFMI is calculated as a FFM adjusted for the squared height, SMI – as a skeletal muscle mass adjusted for the squared height. These indices are the most informative for the diagnosis of skeletal muscle dysfunction, because it excludes the effect of fat tissue on results.

All patients filled out the St. George's Respiratory Questionnaire (SGRQ) by themselves with the official Ukrainian translations.[23] According to this questionnaire, the following components of the quality of life were calculated: total – the impact of the disease on overall health status; symptoms – the effect of respiratory symptoms, their frequency and severity; activity – the activities that cause or are limited by breathlessness; and impact – the aspects concerned with social functioning and the impact of psychological problems.

Descriptive statistics were used to characterize the population.

Obtained anamnestic data, patient survey results, and questionnaire data were formed in the order and interval scales of statistical data. According to the Kolmogorov–Smirnov test, they were not subject to normal data distribution. Therefore, the rank correlation was calculated according to the Spearman criterion. Stepwise multiple regression analysis was performed.


   Results Top


The mean frequency of the COPD exacerbations was quite high (2.3 ± 1.4/year), which corresponds to the prevalence of Groups C and D among the patients.

According to the results of the examination of the skeletal muscles, functional status and muscle mass were reduced [Table 1]. Handgrip strength of the muscles was only 77.6% ± 18.6% of the age norm, and the distance of 6MWT was 319.1 ± 111.2 m, that was significantly different from the proper indicators, which according to Bohannon must exceed 600 m.[24] FFMI and SMI were accordingly 19.4 ± 2.6 kg/m2 and 8.5 ± 1.5 kg/m2, which corresponds to previously published by Ischaki et al. research on the determination of these indicators in the population of COPD patients.[25]

Results of the statistical analysis of the obtained data are shown in [Table 2]. By calculating the rank correlation using Spearman criterion, we identified the number of correlations with different strength. Thus, we found a weak negative correlation between the growing of the COPD exacerbation frequency and 6MWT distance (r = −0.214; P = 0.034) [Figure 1].
Table 2: Correlation between the chronic obstructive pulmonary disease exacerbations and the morphofunctional characteristics of skeletal muscles

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Figure 1: Correlation between the frequency of the chronic obstructive pulmonary disease exacerbations and the 6-min walking test distance

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It was found that frequency of the COPD exacerbations had a weak negative correlation with the FFMI (r = −0.201; P = 0.047) [Figure 2].
Figure 2: Correlation between the frequency of the chronic obstructive pulmonary disease exacerbations and the Fat-Free Mass Index

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After assessment of the life quality components, according to the SGRQ, a weak-positive correlation between the frequency of the COPD exacerbations and the impact of the disease on overall health status (r = 0.478; P < 0.001) and all its components were found: the activities that cause or are limited by breathlessness (r = 0.436; P < 0.001), the effect of respiratory symptoms, their frequency and severity (r = 0.395; P < 0.001), and the aspects concerned with social functioning and the impact of psychological problems (r = 0.41; P < 0.001) [Table 2]. In a step-wise multiple regression analysis, total score (partial R2 = 0.048, P < 0.0001) was positively related to frequency of COPD exacerbations.


   Discussion Top


Our study aimed to determine whether the frequency of the COPD exacerbations affects the degree of the skeletal muscle dysfunction in patients with COPD and to determine which characteristics of the muscles will reflect this effect.

According to these tasks, we found that in COPD patients with frequent exacerbations, the degree of SMD was significantly greater than in those who had exacerbations less frequently [Table 2]. Hence, the increase in the frequency of COPD exacerbations negatively affects the functional state of skeletal muscles by reducing exercise tolerance on the basis of the 6MWT results. Pitta et al. in their study also point out that according to the daily monitoring of physical activity in patients who suffered the COPD exacerbation, even in a month after the completion of treatment in the hospital, there was a decrease in walking time compared with stable patients.[26] Alahmari et al. had shown a decrease in the 6MWT distance of patients during exacerbation and for 3–7 days after the exacerbation.[16]

Regarding the effect of exacerbation on the skeletal muscle mass, it should be noted that this issue is much less studied. Hopkinson et al. proved the presence of a negative correlation between the frequency of the COPD exacerbations and FFM,[27] and also found out that the decrease of the FFM in COPD patients was associated with the deterioration of the airflow limitation and poor quality of life. Martínez-Llorens et al., using bioelectric impedance analysis, found a significant difference in the size of the skeletal muscle of persons hospitalized for COPD exacerbation and stable patients.[28] Vilaró et al. established on the basis of the FFM, that the degree of the skeletal muscle dysfunction strongly correlated with the presence of previous or present exacerbation of COPD.[29] The results of our study coincide with these data and indicate that the rise in the frequency of exacerbations is negatively reflected in the skeletal muscles mass. Thus, the decrease of the FFMI by the results of bioelectric impedance analysis is associated with frequent exacerbations [Table 2].

The results of our study did not reveal a significant difference in the skeletal muscle strength in patients with frequent and rare COPD exacerbations [Table 1], which differs from a number of previously published works. Kazuya et al. had shown that there is a correlation between the frequency of COPD exacerbations and strength of the erector spinae muscles.[30] Vilaró et al. proved that in patients who were often hospitalized in case of the COPD exacerbations, the handgrip dynamometry results were significantly lower than those with stable COPD.[29] Of course, there are data, and our own observations confirm them, regarding the effect of the COPD exacerbation on muscle strength during exacerbation and in the short period after discharge from the hospital. Alahmari et al. found the reduction of the quadriceps femoris muscle strength during COPD exacerbation and within 7 days after that.[16] However, according to the Spruit et al. data, this negative effect on the skeletal muscle was maintained for about 90 days, after which the strength of skeletal muscle restores to previous values.[31] That is, in the study of our group of COPD patients, the decrease in muscle strength due to the COPD exacerbation could only be observed in patients who suffered from it in the last 3 months, as result of which correlation have not been confirmed.

Decrease of the life quality during the COPD exacerbations well studied by many scientists such as Roche et al.[32] and Menn et al.[33] Nevertheless, our study found out that the life quality of patients in the period between exacerbations depends on the overall frequency of the COPD exacerbations over the past year [Table 1]. That is, the deterioration in the quality of life, which occurs during exacerbation, remains extremely long. This negative impact on the overall quality of life is due to negative effects on all life quality components, but most severe due to the activities that cause or are limited by breathlessness. Quite a few scientific researches have been studying this issue. Among them, we should highlight Steer et al. who found that the reduced components of life quality were restored to the baseline level in 3 months after exacerbation, except for the activities that cause or are limited by breathlessness – for a complete recovery of which it takes 6 months.[34] Andenaes et al. had shown that exacerbation was such a severe physiological stress for the body that improving the quality of life above the level before exacerbation was possible in patients only in 9 months after the COPD exacerbation.[35]


   Conclusions Top


We found that COPD exacerbation has an important role in the progression of skeletal muscle dysfunction. As a result of the frequent exacerbations, there is a decrease in endurance of skeletal muscles diminishing their size, which manifests itself in reduced exercise tolerance. In addition, due to the increase in the restriction of the physical activity in patients with more frequent COPD exacerbations, there is a decline in all components of the life quality.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Casaburi R. Skeletal muscle dysfunction in chronic obstructive pulmonary disease. Med Sci Sports Exerc 2001;33:S662-70.  Back to cited text no. 1
    
2.
Shrikrishna D, Patel M, Tanner RJ, Seymour JM, Connolly BA, Puthucheary ZA, et al. Quadriceps wasting and physical inactivity in patients with COPD. Eur Respir J 2012;40:1115-22.  Back to cited text no. 2
    
3.
Wüst RC, Morse CI, de Haan A, Rittweger J, Jones DA, Degens H, et al. Skeletal muscle properties and fatigue resistance in relation to smoking history. Eur J Appl Physiol 2008;104:103-10.  Back to cited text no. 3
    
4.
De Theije CC, Schols A, Lamers WH, Kohler SE, Langen RCJ. Hypoxia sensitizes skeletal muscle to fasting-induced muscle atrophy; role of AMPK activation. European Respiratory Journal 2015;46:2.  Back to cited text no. 4
    
5.
Jaitovich A, Angulo M, Lecuona E, Dada LA, Welch LC, Cheng Y, et al. High CO2 levels cause skeletal muscle atrophy via AMP-activated kinase (AMPK), foxO3a protein, and muscle-specific ring finger protein 1 (MuRF1). J Biol Chem 2015;290:9183-94.  Back to cited text no. 5
    
6.
Puig-Vilanova E, Rodriguez DA, Lloreta J, Ausin P, Pascual-Guardia S, Broquetas J, et al. Oxidative stress, redox signaling pathways, and autophagy in cachectic muscles of male patients with advanced COPD and lung cancer. Free Radic Biol Med 2015;79:91-108.  Back to cited text no. 6
    
7.
Bodine SC, Furlow JD. Glucocorticoids and skeletal muscle. In: Glucocorticoid Signaling. New York, NY: Springer; 2015. p. 145-76.  Back to cited text no. 7
    
8.
Schols AM, Ferreira IM, Franssen FM, Gosker HR, Janssens W, Muscaritoli M, et al. Nutritional assessment and therapy in COPD: A European Respiratory Society statement. Eur Respir J 2014;44:1504-20.  Back to cited text no. 8
    
9.
Agustí AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X, et al. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J 2003;21:347-60.  Back to cited text no. 9
    
10.
Gupta M, Vardey SK, Sinha M, Joshi N, Dixit R, Gupta R. Evaluation of anabolic hormone status in patients with COPD during stable and acute exacerbation state. Biomedical Research-India 2014;25:371-6.  Back to cited text no. 10
    
11.
Beaudart C, Buckinx F, Rabenda V, Gillain S, Cavalier E, Slomian J, et al. The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: A systematic review and meta-analysis of randomized controlled trials. J Clin Endocrinol Metab 2014;99:4336-45.  Back to cited text no. 11
    
12.
Wedzicha JA, Seemungal TA. COPD exacerbations: Defining their cause and prevention. Lancet 2007;370:786-96.  Back to cited text no. 12
    
13.
Andelid K, Glader P, Yoshihara S, Andersson A, Ekberg-Jansson A, Linden A. Hypoxia associated with increased systemic concentrations of MPO and NE during exacerbations of COPD. European Respiratory Journal 2015;46.  Back to cited text no. 13
    
14.
Abroug F, Ouanes-Besbes L, Hammouda Z, Benabidallah S, Dachraoui F, Ouanes I, et al. Noninvasive ventilation with helium-oxygen mixture in hypercapnic COPD exacerbation: Aggregate meta-analysis of randomized controlled trials. Ann Intensive Care 2017;7:59.  Back to cited text no. 14
    
15.
Girón R, Matesanz C, García-Río F, de Santiago E, Mancha A, Rodríguez-Salvanés F, et al. Nutritional state during COPD exacerbation: Clinical and prognostic implications. Ann Nutr Metab 2009;54:52-8.  Back to cited text no. 15
    
16.
Alahmari AD, Kowlessar BS, Patel AR, Mackay AJ, Allinson JP, Wedzicha JA, et al. Physical activity and exercise capacity in patients with moderate COPD exacerbations. Eur Respir J 2016;48:340-9.  Back to cited text no. 16
    
17.
Perera WR, Hurst JR, Wilkinson TM, Sapsford RJ, Müllerova H, Donaldson GC, et al. Inflammatory changes, recovery and recurrence at COPD exacerbation. Eur Respir J 2007;29:527-34.  Back to cited text no. 17
    
18.
Stanojkovic I, Kotur-Stevuljevic J, Milenkovic B, Spasic S, Vujic T, Stefanovic A, et al. Pulmonary function, oxidative stress and inflammatory markers in severe COPD exacerbation. Respir Med 2011;105 Suppl 1:S31-7.  Back to cited text no. 18
    
19.
Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J 2005;26:319-38.  Back to cited text no. 19
    
20.
Massy-Westropp NM, Gill TK, Taylor AW, Bohannon RW, Hill CL. Hand grip strength: Age and gender-stratified normative data in a population-based study. BMC Res Notes 2011;4:127.  Back to cited text no. 20
    
21.
Singh SJ, Puhan MA, Andrianopoulos V, Hernandes NA, Mitchell KE, Hill CJ, et al. An official systematic review of the European Respiratory Society/American Thoracic Society: Measurement properties of field walking tests in chronic respiratory disease. Eur Respir J 2014;44:1447-78.  Back to cited text no. 21
    
22.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39:412-23.  Back to cited text no. 22
    
23.
Ringbaek T, Martinez G, Lange P. A comparison of the assessment of quality of life with CAT, CCQ, and SGRQ in COPD patients participating in pulmonary rehabilitation. COPD 2012;9:12-5.  Back to cited text no. 23
    
24.
Bohannon RW. Six-minute walk test: A meta-analysis of data from apparently healthy elders. Top Geriatr Rehabil 2007;23:155-60.  Back to cited text no. 24
    
25.
Ischaki E, Papatheodorou G, Gaki E, Papa I, Koulouris N, Loukides S, et al. Body mass and fat-free mass indices in COPD: Relation with variables expressing disease severity. Chest 2007;132:164-9.  Back to cited text no. 25
    
26.
Pitta F, Troosters T, Probst VS, Spruit MA, Decramer M, Gosselink R, et al. Physical activity and hospitalization for exacerbation of COPD. Chest 2006;129:536-44.  Back to cited text no. 26
    
27.
Hopkinson NS, Tennant RC, Dayer MJ, Swallow EB, Hansel TT, Moxham J, et al. Aprospective study of decline in fat free mass and skeletal muscle strength in chronic obstructive pulmonary disease. Respir Res 2007;8:25.  Back to cited text no. 27
    
28.
Martínez-Llorens JM, Orozco-Levi M, Masdeu MJ, Coronell C, Ramírez-Sarmiento A, Sanjuas C, et al. Global muscle dysfunction and exacerbation of COPD: A cohort study. Med Clin (Barc) 2004;122:521-7.  Back to cited text no. 28
    
29.
Vilaró J, Ramirez-Sarmiento A, Martínez-Llorens JM, Mendoza T, Alvarez M, Sánchez-Cayado N, et al. Global muscle dysfunction as a risk factor of readmission to hospital due to COPD exacerbations. Respir Med 2010;104:1896-902.  Back to cited text no. 29
    
30.
Tanimura K, Sato S, Sato A, Hasegawa K, Uemasu K, Hamakawa Y, et al. Frequent Exacerbations Of COPD Cause Loss Of Antigravity Muscles - Quantitative And Longitudinal Analysis Using Chest CT. American Journal of Respiratory and Critical Care Medicine 2016;193.  Back to cited text no. 30
    
31.
Spruit MA, Gosselink R, Troosters T, Kasran A, Gayan-Ramirez G, Bogaerts P, et al. Muscle force during an acute exacerbation in hospitalised patients with COPD and its relationship with CXCL8 and IGF-I. Thorax 2003;58:752-6.  Back to cited text no. 31
    
32.
Roche N, Wedzicha JA, Patalano F, Frent S-M, Larbig M, Shen S, et al. COPD exacerbations significantly impact quality of life as measured by SGRQ-C total score: results from the FLAME study. European Respiratory Journal 2017;50(Suppl 61):OA1487.  Back to cited text no. 32
    
33.
Menn P, Weber N, Holle R. Health-related quality of life in patients with severe COPD hospitalized for exacerbations – Comparing EQ-5D, SF-12 and SGRQ. Health Qual Life Outcomes 2010;8:39.  Back to cited text no. 33
    
34.
Steer J, Gibson GJ, Bourke SC. Longitudinal change in quality of life following hospitalisation for acute exacerbations of COPD. BMJ Open Respir Res 2015;2:e000069.  Back to cited text no. 34
    
35.
Andenaes R, Moum T, Kalfoss MH, Wahl AK. Changes in health status, psychological distress, and quality of life in COPD patients after hospitalization. Qual Life Res 2006;15:249-57.  Back to cited text no. 35
    


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