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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 3  |  Issue : 3  |  Page : 701-708

Chronic obstructive pulmonary disease and ultrasonographic assessment of quadriceps muscle


1 Department of Chest Diseases, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt
2 Department of Rheumatology & Rehabilitation, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt

Date of Submission15-Oct-2019
Date of Decision15-Oct-2019
Date of Acceptance26-Nov-2019
Date of Web Publication10-Feb-2020

Correspondence Address:
MD Eman Sobh
Chest Diseases Department, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt; Al-Zahraa University Hospital, Abbassia, 11517, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjamf.sjamf_86_19

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  Abstract 


Introduction Quadriceps muscle (QM) dysfunction has been recognized as a major cause of impaired physical activity in patients with chronic obstructive pulmonary disease (COPD). Clinical assessment of muscle power is not fully accurate in differentiating the degree of impairment. The use of muscle ultrasound has been introduced to study extrapulmonary complications in COPD such as diaphragm and limb muscle impairment.
Aim To assess the relationship between severity of COPD and ultrasonographic assessment of QM and its strength by dynamometer.
Patients and methods This prospective observational case–control study was conducted on 100 patients with stable COPD attending Chest Diseases Outpatient Clinic and 100 healthy controls with normal lung functions from December 2017 to June 2019. Spirometry, arterial blood gases, and 6-min walking distance were done for all cases. A hand-held dynamometer was used to measure QM strength. Ultrasonography was used to evaluate QM subcutaneous fat, quadriceps muscle thickness (QMT), and rectus femoris cross-sectional area (RFCSA).
Results Patients with COPD had significantly lower QM clinical power and strength by dynamometer and decreased QMT and RFCSA in comparison with controls. Overall, 89% of patients with COPD had decreased QM strength by dynamometer, 68% had decreased QMT, and 67% had decreased RFCSA. Most of the patients with COPD who experienced QM weakness were older, had low body mass, had more severe airway obstruction, had more advanced COPD stage, and had lower quality-of-life scores. Life space activity (LSA) score, thigh circumference, and maximum voluntary volume were the factors that had significant effect on RFCSA. However, disease duration, dyspnea score, COPD Assessment Test score, LSA score, and thigh circumference had significant effect on QMT. Meanwhile, LSA and maximum voluntary volume had significant effect on QM strength.
Conclusion Most patients with COPD had QM weakness and are associated with more advanced disease and worse quality of life. These findings are important and indicate that peripheral muscle assessment should be incorporated into the clinical assessment of COPD.

Keywords: chronic obstructive pulmonary disease, hand-held dynamometer, quadriceps muscle strength, quadriceps muscle ultrasonography, quadriceps muscle weakness, skeletal muscle dysfunction, spirometry


How to cite this article:
Abdellateef HS, Ahmed ES, Adawy ZR, Elabd H, Sobh E. Chronic obstructive pulmonary disease and ultrasonographic assessment of quadriceps muscle. Sci J Al-Azhar Med Fac Girls 2019;3:701-8

How to cite this URL:
Abdellateef HS, Ahmed ES, Adawy ZR, Elabd H, Sobh E. Chronic obstructive pulmonary disease and ultrasonographic assessment of quadriceps muscle. Sci J Al-Azhar Med Fac Girls [serial online] 2019 [cited 2020 Feb 29];3:701-8. Available from: http://www.sjamf.eg.net/text.asp?2019/3/3/701/278050




  Introduction Top


Chronic obstructive pulmonary disease (COPD) is associated with comorbidities that can influence prognosis [1]. Skeletal muscle dysfunction and wasting are one of the most significant comorbidities in COPD [2]. It has been reported that skeletal muscle dysfunction in COPD is an important cause of increasing dyspnea and impaired quality of life [3]. Loss of function of lower limb muscles [4], especially quadriceps muscle (QM) weakness, is the most prevalent type of skeletal muscle impairment [5]. It affects nearly one-third of patients with COPD [5]. Skeletal muscle weakness may be attributed to several factors including physical inactivity owing to dyspnea and associated comorbidities [6], systemic inflammatory response [7],[8], systemic corticosteroids [9], genetic predisposition [10], an imbalance between catabolic and anabolic hormones, nutritional depletion, and protein degradation [11]. Skeletal muscle training was reported to improve dyspnea and quality-of-life scores and pulmonary functions in some studies [12]. Therefore, the assessment of QM in patients with COPD is important in the management plan of the disease.


  Aim Top


The aim of this study was to assess the relationship between severity of COPD and ultrasonographic assessment of QM and its strength by dynamometer.


  Patients and methods Top


Study design

This prospective observational case–control study was conducted on 100 patients with COPD and an equal number of healthy controls. Patients with COPD were selected from chest diseases outpatient clinic at Al-Zahraa University Hospital, Cairo, Egypt, in the period from December 2017 to June 2019. The sample size was calculated using Kelsey method [13] (open Epic calculator, version 3, available at https://www.openepi.com/SampleSize/SSCC.htm), which revealed that the required sample was 88 patients for each group.

Inclusion criteria

Chronic obstructive pulmonary disease group

Diagnosis of patients with COPD was based on criteria established by GOLD 2018 [14]. They were stable and had no acute exacerbation of symptoms within the past 4 weeks before the study.

Control group

Healthy volunteers were age and sex matched and had normal spirometry results.

Exclusion criteria

Patients who were affected by neuromuscular disease, had a history of lower limb surgery, were clinically unstable for at least 4 weeks before the visit, or walked with an assistive device had been excluded.

Ethical considerations

The ethical committee board of the Faculty of Medicine for Girls, Al-Azhar University (AFMG-IRB) approved the study protocol. A written informed consent was taken from all participants after proper explanation of the study.

All participants were subjected to the following:
  1. Medical history and clinical examination: including the recording of demographic data such as age, sex, smoking status, drug, occupation, disease duration, and the presenting symptoms. Dyspnea was assessed using modified Medical Research Council (mMRC) dyspnea scale [15]. Other symptoms were recorded using the COPD Assessment Test (CAT) score [16]. Life-space assessment (LSA) [17] was used to assess quality of life for all participants. We recorded also, weight (kg), height (m2), BMI (kg/m2), and mid-thigh cross-sectional area (cm).
  2. Spirometry was carried out for using spirometer device (Spiro sift SP-5000, FUKUDA Nish). Values of pulmonary function test including forced expiratory volume in 1 s (FEV1), vital capacity (VC), forced vital capacity (FVC), maximum voluntary volume (MVV), forced expiratory flow (FEF25–75), FEV1/FVC were calculated using best out of three technically acceptable performances, in agreement with the recommendations of the European Respiratory Society [18]. Post bronchodilator test was performed for patients with COPD after inhalation of 0.4 mg salbutamol to exclude asthmatic patients. Severity of COPD was classified by both GOLD stage into mild, moderate, severe, and very severe based on post bronchodilator FEV1 (>80%, 50–80%, 30–50%, and < 30%, respectively) and new GOLD classification (A/B/C/D) based on combined symptoms and exacerbation history [14].
  3. Arterial blood gases samples from patients with COPD were analyzed using blood gas analyzer (RAPIDLAB 248; Siemens Healthcare Diagnostics Inc., Malvern, PA, US).
  4. Exercise testing: 6-min walk test was used to measure the lower limb functional capacity. It was done according to the ATS guidelines [19]. Oxygen saturation and pulse rate were assessed at the start and end of the test by pulse oximetry. The distance [6-min walking distance (6MWD)] (m) was recorded at the end of the 6 min.
  5. Routine investigations: complete blood count, liver function tests, kidney function tests, and serum glucose level were obtained from recent patients’ files to exclude patients with any debilitating disease.
  6. QM assessment was done, including the following measures:
    1. Clinical assessment of knee tone to exclude patients with hypotonia or hypertonia.
    2. Manual Muscle Testing: the patient was asked to extend the knee against tester’s resistance, and the grade was scored based on a five-point grading scale, from zero, no visible or palpable muscle contraction; ‘grade 3’, limb movement against gravity without resistance; to ‘grade 5,’ muscle contraction against the tester’s full manual resistance [20].
    3. QM strength assessment: QM strength was objectively measured using a hand-held dynamometer (Baseline Push Pull Force Gauge) (kg). The patient was sitting at the side of the treatment table with the leg tested at 90° of knee flexion [21]. A break test, where the tester overcomes to the patient’s force [20], was performed in this position over the course of 5 s. The mean of three trials was recorded (kg) on each leg.
    4. Ultrasonographic assessment of QM: US scanning was performed with Soundscape A8 Medical Systems (Shenzhen, China), using a linear transducer (10 MHz) and B-mode. The participants were asked to be in the supine position, with the lower limbs naked and relaxed completely. All scans were made through the QM halfway along the line from the anterior–superior iliac spine to the superior aspect of the patella [22]. The gain (83 dB), depth (6 cm), time gain compensation (in the neutral position), and focus were kept constant between patients. To show the best bone echo, the transducer was always perpendicular to the targeted muscle [23]. Minimum pressure was maintained at the transducer to avoid distortion of the skin and subcutaneous tissues using an adequate amount of contact gel [24]. On a frozen image, the rectus femoris cross-sectional area (RFCSA) was calculated by tracing the inner outline of the rectus femoris manually using a movable cursor. Quadriceps muscle thickness (QMT) was measured as the vertical distance from fascia of the rectus femoris to the underlying femur. The subcutaneous fat thickness of the anterior compartment of the mid-thigh was defined as the distance between the dermis and fascia of the rectus femoris muscle ([Figure 1]).
      Figure 1 Ultrasonographic assessment of quadriceps muscle (left image shows the technique; right image shows ultrasonographic image).

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Statistical analysis

Data were collected, coded, tabulated, revised, and statistically analyzed and entered using Statistical Package for Social Science version 20 (SPSS, IBM Corp., Armonk, New York, USA). c2 test and Fisher exact test were used for categorical variables as indicated. Independent t test and Mann–Whitney test were used for comparing quantitative data with parametric and nonparametric distributions, respectively. Spearman correlation coefficients were used to assess the significant relation between two quantitative parameters in the same group. Regression analysis was done to detect factors affecting QM parameters. The confidence interval was set to 95%, and the margin of error accepted was set to 5%. Level of significance was considered at P value less than 0.05.


  Results Top


We evaluated 890 patients, and 510 were eligible; of them, 210 agreed to participate in the study. Cases with missed data or declined to consent were excluded. We allocated participants into COPD group or control group according to the inclusion criteria. Final analysis involved 100 patients with COPD diagnosed according to GOLD 2018 criteria [14] and 100 age-matched and sex-matched healthy participants as a control group. The consort of the study is shown in [Figure 2].
Figure 2 The CONSORT diagram of the study.

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Most of the studied populations were male in both groups (94%). Patients with COPD had significant impairment of pulmonary functions, quality of life and physical activity scores, and 6MWD. Demographic data and basic characteristics of the studied groups are shown in [Table 1] and [Table 2].
Table 1 Demographic data and basic characteristics of the studied population

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Table 2 Other characteristics of chronic obstructive pulmonary disease group

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There was a statistically significant reduction in QM clinical power, strength by a dynamometer [quadriceps maximum voluntary contraction (QMVC)], and ultrasonographic parameters (RFCSA and QMT) in COPD group in comparison with control one ([Table 3]).
Table 3 Quadriceps muscle assessment of the studied groups by different methods

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There was a significant positive linear correlation of quadriceps strength with RFCSA and QMT in both control and COPD groups ([Figure 3] and [Figure 4]). Moreover, RFCSA showed significant positive linear correlation with QMT in both groups ([Table 4] and [Table 5]).
Figure 3 Correlation between quadriceps muscle strength by dynamometer and rectus femoris muscle cross-sectional area in COPD group. COPD, chronic obstructive pulmonary disease.

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Figure 4 Correlation between quadriceps muscle strength by dynamometer and quadriceps muscle thickness in COPD group. COPD, chronic obstructive pulmonary disease.

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Table 4 Correlation of quadriceps muscle assessment with some variables in control group

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Table 5 Correlation of quadriceps muscle assessment with some variables in chronic obstructive pulmonary disease group

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There was a significant positive correlation between QM strength by dynamometer and height, LSA score, clinical power of lower limb, 6MWD, FEV1/FVC, VC%, FVC%, FEV1%, FEF25–75%, and MVV% in both control group and COPD group, whereas it was negatively correlated with age in both groups and with weight and BMI in control group and with duration of COPD, mMRC, CAT score, and BODE in COPD group ([Table 4] and [Table 5]).

RFCSA had significant positive correlation with height, LSA, LL clinical power, 6MWD, FEV1/FVC, VC%, FVC%, FEV1%, FEF25–75%, and MVV% and negative correlation with age in control group. However, in COPD group, there was a significant positive correlation between RFCSA by ultrasonography and height, thigh circumference, LSA, LL clinical power, 6MWD, FEV1/FVC, FEV1%, VC%, FVC%, and FEF25–75%, and MVV%, whereas it was negatively correlated with age, duration of COPD, mMRC, CAT score, and BODE ([Table 4] and [Table 5]).

There was a significant positive correlation of QMT with LSA, height, thigh circumference, clinical power of lower limb, 6MWD, FEV1/FVC, VC%, FVC%, FEV1%, FEF25–75%, and MVV%, and it was negatively correlated with age in control group. However, in COPD group, there was a significant positive correlation between QMT by ultrasound and height, weight, thigh circumference, LSA, LL clinical power, 6MWD, FEV1/FVC, FEV1%, VC%, FVC%, FEF25–75%, and MVV%, whereas it was negatively correlated with age, duration of COPD, mMRC dyspnea score, CAT score, and BODE index ([Table 4] and [Table 5]).

In this study, we found 89% of patients with COPD had decreased QM strength by dynamometer, whereas ultrasound detected 68% (more than three-quarters of those detected by dynamometer) of decreased QM mass. Patients with QM impairment were older, had low body mass, had more severe airway obstruction and more advanced COPD stage, and had lower quality-of-life scores. Regression analysis revealed factors that had significant effect on RFCSA were LSA score, thigh circumference, and MVV, and the factors having significant effect on QMT were disease duration, dyspnea score, CAT score, LSA, and thigh circumference, whereas the factors having significant effect on QM strength are LSA and MVV.


  Discussion Top


In this study, we evaluated QM function in patients with COPD in comparison with control group using different methods; we measured the clinical power, the QMVC by dynamometer, and QMT and RFCSA by ultrasound. The main finding of this study was that there is a significant decrease in QM power, strength, and ultrasonographic parameters when compared with control group ([Table 3]). Similar results were reported in previous studies [8],[24],[25],[26],[27]. Skeletal muscle dysfunction in COPD may be owing to the systemic inflammatory response of COPD, physical inactivity, associated comorbidities in addition to imbalance in nutritional, hormonal, and proteins [4],[28]. Smoking also may be another cause of skeletal muscle disease [29]. In this study, we found 89% of patients with COPD had decreased QM strength by dynamometer whereas ultrasound detected 68% (more than three-quarters of those detected by dynamometer) of decreased QM mass. Previous studies reported similar results. Kharbanda et al. [8] detected that a high number of patients with COPD (92%) had QM weakness using hand-held dynamometer. However, Seymour et al. [5] reported that 32% of UK and 33% of Dutch patients with COPD had quadriceps weakness using isometric QMVC strength by a special device in addition to whole-body and regional (lower-limb) lean mass by dual-energy radiography absorptiometry (DEXABODY and DEXALEG, respectively) in the Dutch cohort. The discrepancy between studies may be owing to the different demographic data and disease severity and the different methods used.

In this study, we found that patients with COPD with QM weakness were older, had lower body weight, had more advanced disease stage, and had bad quality-of-life scores. Similar results were found in Seymour et al. [5], who found more prevalence of QM weakness in advanced stages of COPD (38% in GOLD stage 4).

In this study, regarding QMT in COPD group, there was a significant positive correlation between QMT by ultrasound and height, weight, thigh circumference, LSA, LL clinical power, 6MWD, FEV1/FVC, FEV1%, VC%, FVC%, FEF25–75%, and MVV%, whereas it was negatively correlated with age, duration of COPD, mMRC dyspnea score, CAT score, and BODE index. Seymour et al. [5] found in their study the highest prevalence of weakness was observed in patients with the most severe dyspnea (MRC dyspnea score 4 or 5), and when adjusted to the severity of airflow limitation, severe dyspnea was an independent predictor of QM weakness in the Dutch cohort.

Regression analysis revealed that factors that had significant effect on RFCSA were LSA score, thigh circumference, and MVV, and the factors that had significant effect on QMT were disease duration, dyspnea score, CAT score, LSA, and thigh circumference, whereas the factors that had significant effect on QM strength are LSA and MVV. In the study by Zhang et al. [2], regression analysis indicated that the severity of the decline in functions of the quadriceps femoris and the degree of airflow obstruction in pulmonary function was significantly and positively correlated, suggesting that the decline in function of peripheral skeletal muscle in patients with COPD is a major factor causing limitations of daily activities.

In our study, we used different methods for assessment of QM weakness, so we can detect the sensitivity and specificity of each one.

The limitations include the under-representation of women in our study; however, this reflects the prevalence of COPD and smoking behavior in our country. Although the sample size used was more than the calculated size, the results of small samples could not be generalized, and future studies using a large cohort are warranted.

Conclusion and recommendations

QM dysfunction is prevalent in patients with COPD. Ultrasound is a useful method for assessment of QM; however, it has low sensitivity and specificity compared with the dynamometer. Incorporating QM assessment in the management plan of COPD is recommended.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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