Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 32  |  Issue : 1  |  Page : 198-205

Ultrasonographic assessment of diaphragm in patients with chronic obstructive pulmonary disease in correlation with spirometric parameters


1 Department of Chest, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Menoufia, Egypt
2 Department of Radiology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Menoufia, Egypt

Date of Submission27-Feb-2017
Date of Acceptance09-Apr-2017
Date of Web Publication17-Apr-2019

Correspondence Address:
Rehab A Saad
Damalig Village, Menouf, Menoufia 32951
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_141_17

Rights and Permissions
  Abstract 


Objective
Ultasonographic assessment of the diaphragm in patients with chronic obstructive pulmonary disease (COPD) and studying its correlation with spiromertric parameters.
Background
COPD represents a model of respiratory muscle dysfunction. The diaphragm is the main respiratory muscle, and its assessment is mandatory in the evaluation of patients with COPD. Ultrasonography can be used to assess diaphragmatic thickness, thickening, and excursion.
Patients and methods
This study included 40 patients with COPD and 10 healthy controls. All participants underwent detailed history taking, clinical examination, chest radiographies, 6-min walk test, spirometry [measurement of forced expiratory volume in one second/forced vital capacity (FEV1/FVC), FVC, FEV1, and maximum voluntary ventilation percentage of predicted], and ultrasonographic examination to measure diaphragmatic thickness (TD) at different lung volumes and capacities, thickening, and excursion.
Results
A highly statistically significant difference (P < 0.001) between patients with COPD and controls regarding FEV1/FVC, FEV1, and maximum voluntary ventilation percentage of predicted and a statistically significant difference (P = 0.04) between both groups regarding FVC% of predicted were found. There was a highly statistically significant difference (P < 0.001) among patients with COPD with different grades of severity regarding diaphragmatic thicknesses (TDRV, TDFRC, and TDTLC), diaphragmatic thickening (TDTLCFRC), and diaphragmatic excursion. There was a statistically significant difference (P = 0.002) among different COPD grades regarding diaphragmatic thickening (TDTLCRV). Measurements of diaphragmatic thicknesses (TDFRC and TDTLC) and thickenings (TDTLCRV and TDTLCFRC) decrease significantly in female patients more than in male patients (P = 0.049, 0.031, 0.005, and 0.044, respectively).
Conclusion
Diaphragmatic thickness, thickening, and excursion decrease in patients with COPD and in female more than in male patients. These ultrasonographic measurements negatively correlate with the severity of the disease.

Keywords: chronic obstructive pulmonary disease, diaphragm, ultrasonography


How to cite this article:
Abd El Aziz AA, El Wahsh RA, Abd Elaal GA, Abdullah MS, Saad RA. Ultrasonographic assessment of diaphragm in patients with chronic obstructive pulmonary disease in correlation with spirometric parameters. Menoufia Med J 2019;32:198-205

How to cite this URL:
Abd El Aziz AA, El Wahsh RA, Abd Elaal GA, Abdullah MS, Saad RA. Ultrasonographic assessment of diaphragm in patients with chronic obstructive pulmonary disease in correlation with spirometric parameters. Menoufia Med J [serial online] 2019 [cited 2019 Aug 18];32:198-205. Available from: http://www.mmj.eg.net/text.asp?2019/32/1/198/256084




  Introduction Top


The respiratory muscles show some morphological abnormalities in patients with chronic obstructive pulmonary disease (COPD), which could contribute to their weakness. Subtle changes are present in these patients, such as a decrease in the diameter of individual fibers, variations in fiber size, and splitting of fibers. In addition, in autopsy studies of patients with severe COPD, the diaphragm, the main inspiratory muscle, is reduced in weight greater than would be expected for the reduction in overall body weight in these patients [1].

In comparison with other methods of evaluating diaphragmatic function, ultrasonography has advantages over plain chest radiography and videofluoroscopy, which have high rates of false-positive and false-negative results and transdiaphragmatic pressure measurement, which is invasive, uncomfortable, and only helpful in bilateral paralysis. Needle electromyography of the diaphragm can be very helpful, but it is relatively contraindicated in COPD because of a possible risk of pneumothorax in hyperinflated patients [2].

The aim of this study is to assess the diaphragm in patients with COPD using ultrasonographic examination and to study its correlation with parameters of spirometry.


  Patients and Methods Top


After approval of Menoufia Ethics Committee for the study proposal, this study, 'a retrospective analysis', was carried on 50 individuals: 40 patients with COPD and 10 age-matched and sex-matched controls. Of all patients with COPD who were attending the chest outpatient clinic of Menoufia University Hospital during the period from September 2015 to February 2016, 40 clinically stable patients were chosen: 10 for each severity grade (mild, moderate, severe, and very severe) diagnosed and classified according to Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2016 guideline criteria [3]. Patients with other chest diseases or those with any disease that could affect the diaphragm, e.g., myopathy and neuropathy, or those with recent thoracic or abdominal surgery were excluded from the study. Controls were healthy volunteers who never smoked and were selected from patient's relatives and hospital workers.

All participants, after taking a written consent, underwent full history taking, thorough clinical examination, BMI calculation according to the formula weight (kg)/height (m 2), routine laboratory investigations, and chest radiography. Spirometry was done in the pulmonary function test unit in Menoufia University Hospital using computerized pulmonary function apparatus (Quark PFT 3, COSMED, Rome, Italy). Slow and forced vital capacities (FVC% of predicted), prebronchodilator and post-bronchodilator forced expiratory volume in one second (FEV1% of predicted), FEV1/FVC, and maximum voluntary ventilation (MVV%) of predicted were all measured according to the American Thoracic Society criteria [4]. The best test from three consecutive tests was accepted, and COPD staging was done according to GOLD 2016: mild grade (FEV1 ≥ 80% of predicted), moderate grade (50%≤FEV1 < 80% of predicted), severe grade (30%≤FEV1 < 50% of predicted), and very severe COPD (FEV1 < 30% of predicted). Six minute walk test was then done where patients were motivated to walk in a 35-m long corridor at the fastest speed possible. Oxygen saturation was measured before and after the test, and the distance walked in 6 min was recorded. The collection of BMI, airway obstruction (O) expressed by FEV1% predicted, dyspnea (D) expressed by modified Medical Research Council scale, and exercise capacity (E) expressed by 6-min walk test allows calculation of Bhattacharyya Optical Decoy Evaluation (BODE) index score for each patient by summing the points of each component. All cases underwent ultrasonographic examination of the diaphragm using a ultrasound machine (GE Logiq P5, South Korea, 222 Rampart St., Charlotte, NC 28203). They were examined with a low-frequency curvilinear probe (3.5–5 MHz) in semirecumbent position. For assessment of diaphragmatic thickness (TD) and thickening, TD was measured at the zone of apposition using a technique similar to that presented by Ueki et al. [5], with the probe placed at the anterior axillary line in the intercostal space between seventh and eighth ribs for an 'intercostal view'. B-mode was used to visualize the diaphragm moving toward or away from the transducer. Imaging was then changed to M-mode with the thickness of the hyperechogenic line representing TD that was measured at different lung volumes and capacities – at end of a normal expiration (FRC), during a breath-holding maneuver after maximal inspiration (TLC), and at the end of maximal expiration (RV) – and these were expressed as TDFRC, TDTLC, and TDRV, respectively. The differences between TDTLC and TDFRC (TDTLCFRC) and TDTLC and TDRV (TDTLCRV) were expressed as diaphragmatic thickenings. For assessment of diaphragmatic excursion, the right hemidiaphragm during maximal profound inspiration starting from normal end-expiratory volume was obtained by a technique similar to that reported by Testa et al. [6] with the probe placed between the midclavicular and anterior axillary lines, in the anterior subcostal region for an 'anterior subcostal view'. The diaphragmatic interface appeared in M-mode as a hyperechogenic line that assumed in time a sinusoidal form with the peak representing maximal inspiration and the trough representing expiration. The height of the curve expressed the excursion [Figure 1]. The data then were collected, tabulated, and analyzed by statistical package for the social sciences software version 20 (SPSS Inc., Chicago, Illinois, USA) and Epi Info 2000 programs Epi Info is statistical software for epidemiology developed by Centers for Disease Control and Prevention (CDC) in Atlanta, Georgia (US). Quantitative data were expressed as mean ± SD and analyzed by applying t-test for comparison between two groups with parametric variables, Mann–Whitney test for comparison between two groups of nonparametric variables, analysis of variance (F-test) for comparison between multiple groups with parametric variables, and Kruskal–Wallis test for comparison between multiple groups with nonparametric variables. Qualitative data was expressed as numbers and percentages, and χ2) was applied to study association between two qualitative variables.
Figure 1: Ultrasonography of a male patient with very severe chronic obstructive pulmonary disease showing diaphragmatic thickness at residual volume, functional residual capacity, total lung capacity, and diaphragmatic excursion.

Click here to view



  Results Top


In the present study, males predominated females, as 75% of patients were males; eight (80%) in mild COPD group, seven (70%) in moderate group, seven (70%) in severe group, and eight (80%) in very severe group were males, with a statistically insignificant difference among the four groups regarding age and sex [Table 1].
Table 1: Statistical comparison of demographic data among patients with chronic obstructive pulmonary disease with different grades of severity (n=40)

Click here to view


A highly statistically significant difference was found between patients with COPD and controls regarding FEV1/FVC, FEV1, and MVV% of predicted (P < 0.001), with the mean values in patients being 47.4 ± 15.92, 51.8 ± 21.27, and 51.4 ± 16.47, respectively. The mean values of FEV1/FVC, FEV1, and MVV% predicted of controls were 86.8 ± 4.92, 96.4 ± 10.04, and 94.4 ± 15.17, respectively. There was also a statistically significant difference between both groups regarding FVC % of predicted (P = 0.04) where the mean value was 84.9 ± 8.1 and that of controls was 91.2 ± 10.67 [Table 2].
Table 2: Statistical comparison of spirometric results between patients with chronic obstructive pulmonary disease and control group

Click here to view


FEV1% of predicted, FEV1/FVC, and MVV% of predicted varied among the four subgroups of patients with COPD with the least results in very severe COPD group with mean values of 27.2, 27.9 and 36.0%, respectively.

On the contrary, there was no significant variation among them regarding FVC% of predicted, with the least results in very severe COPD (80.5%), which was still within the normal ranges [Figure 2] and [Figure 3].
Figure 2: Statistical comparison of spirometric results (forced expiratory volume in one second of predicted and forced vital capacity of predicted) among the patients with four severity groups of chronic obstructive pulmonary disease.

Click here to view
Figure 3: Statistical comparison of spirometric results (forced expiratory volume in one second/forced vital capacity and maximum voluntary ventilation percentage percentage of predicted) among the patients with four severity groups of chronic obstructive pulmonary disease.

Click here to view


A highly statistically significant difference was found among patients with COPD with different grades of severity regarding BMI and BODE index (P < 0.001), where the lowest BMI (mean: 21.5 ± 3.26 kg/m 2) and the highest BODE index (mean: 6.60 ± 0.52) were found in patients with very severe COPD [Table 3].
Table 3: Statistical comparison of BMI and BODE index among patients with chronic obstructive pulmonary disease with different grades of severity (n=40)

Click here to view


Ultrasonographic measurements of diaphragmatic thickness, thickening, and excursion were found to vary significantly between patients with COPD and controls, with less values in patients with COPD [Figure 4] and [Figure 5].
Figure 4: Statistical comparison of ultrasonographic findings (diaphragmatic thickness –TDRV, TDFRC, and TDTLC) between patients with chronic obstructive pulmonary disease and control group.

Click here to view
Figure 5: Statistical comparison of ultrasonographic findings (diaphragmatic thickenings and excursion) between patients with chronic obstructive pulmonary disease and control group.

Click here to view


A statistically significant difference was found between male and female patients with COPD regarding diaphragmatic thicknesses (TDFRC and TDTLC) and thickenings (TDTLCRV and TDTLCFRC) (P = 0.049, 0.031, 0.005, and 0.044, respectively). On the contrary, there was a statistically insignificant difference between them regarding TDRV and excursion (P = 0.10 and 0.17, respectively) [Table 4].
Table 4: Statistical comparison of ultrasonographic findings between male and female patients with chronic obstructive pulmonary disease

Click here to view


A highly statistically significant difference (P < 0.001) was found among patients with COPD with different grades of severity as regarding ultrasonographic measurements of diaphragmatic thicknesses, thickening (TDTLCFRC), and excursion, with the lowest measurements in very severe group. A significant difference was also found among them regarding TDTLCRV (P = 0.002) [Table 5] and [Figure 2], [Figure 3]. Comparison between each group and other severity groups regarding ultrasonographic findings is shown in [Table 6].
Table 5: Statistical comparison of ultrasonographic measurements among the studied groups (n=40)

Click here to view
Table 6: Post hoc least significant difference of ultrasonographic findings among patients with chronic obstructive pulmonary disease with different grades of severity (n=40)

Click here to view



  Discussion Top


The GOLD 2016 recommends spirometry as the gold standard for COPD diagnosis. Airflow limitation is best measured by spirometry, as this is the most reproducible test of pulmonary function [3]. However, spirometry requires patients' cooperation and depends on their efforts. Owing to these problems, it is not widely used by general practitioners, and COPD under diagnosis is frequent. Therefore, another screening method is needed [7],[8]. Ultrasonography has the advantages of being independent of the patients' efforts or understanding of the procedure, together with precise measurements and real-time assessment. In patients with COPD, noninvasive assessment of the diaphragmatic kinetics from ultrasound measurements of the thickness, thickening, and excursion could be a reliable and beneficial method to estimate the severity of the disease.

In this study, males predominated females, as 75% of patients were males.

This can be explained by the fact that COPD is a male-dominant disease, which may be related to the higher prevalence of smoking and the frequent occupational exposures in them.

This was in agreement with Sorheim et al. [9] and Kim et al. [10] who found that COPD prevalence was higher in men owing to the sex-related differences in sensitivity to smoking and airway anatomy.

In the present study, there was a highly statistically significant difference between patients with COPD and controls regarding FEV1% of predicted and FEV1/FVC. These parameters were found to vary among the different COPD grades and decrease with the progress of the disease, with the lowest values in patients with very severe COPD.

This coincides with GOLD-based criteria of diagnosis that defined COPD as the presence of airflow limitation evidenced by FEV1/FVC less than 0.7 with poor bronchodilator reversibility and classified into four grades according to the severity of airflow limitation based on post-bronchodilator FEV1% of predicted.

In the current study, MVV% of predicted was highly significantly different between patients with COPD and controls and decreased with the advancement of COPD with the lowest results in patients with very severe COPD.

This indicates that the elastic and flow-resistive properties of the respiratory system and respiratory muscle strength were defective in patients with COPD.

In the present study, there was a highly statistically significant difference among patients with COPD with different grades of severity regarding BMI with the lowest index in very severe group.

This was in agreement with Decramer et al. [11] who studied the systemic effects of COPD and found that BMI decreases with the progress of the disease.

This can be explained by the presence of systemic effects of COPD as osteoporosis and nutritional imbalance. In some patients, severe disease may cause a low BMI from the progressing dyspnea, inflammation, and hypoxia, which further increases energy consumption and finally results in nutritional depletion and loss of weight [11].

These results were against those of Franssen et al. [12] and Ora et al. [13] who found an association between obesity or morbid obesity and COPD.

Zammit et al. [14] found that the classic clinical COPD phenotype, including 'blue bloater', was typically associated with chronic bronchitis in overweight persons. They explained their results that obesity is also highly related to chronic and low-grade inflammation that may contribute to the development of COPD. However, Guerra et al. [15] had suggested that a low BMI was related to emphysema whereas obesity was related to chronic bronchitis.

In the present study, BODE index was highly significantly different among patients with COPD with different grades of severity with the lowest index in mild group and the highest index in patients with very severe COPD, i.e., BODE index could express the severity of the disease.

These results were in agreement with those of Sarioglu et al. [16] and Ong et al. [17] who showed that the BODE index was a significant determinant for the severity of COPD exacerbations with respect to FEV1 alone.

This could be explained by the effect of FEV1 in both GOLD staging and BODE index. COPD is regarded as a systemic disease causing structural and functional changes in the lung and other organs. Weight loss and weakness of peripheral muscles are examples of these systemic consequences that could affect the quality of life and exercise tolerance of the patients [18],[19].

In the current work, patients also underwent ultrasonographic assessment of diaphragmatic thickness, thickening, and excursion.

Diaphragmatic thicknesses (TDFRC and TDTLC) and diaphragmatic thickenings (TDTLCRV and TDTLCFRC) in patients with COPD were found to be significantly greater in males than in females.

These results were in agreement with Harper et al. [20], Cohn et al. [21], and Smargiassi et al. [22] whose studies showed sex variability in ultrasonographic measurements, with greater thicknesses and thickenings in males than in females.

The possible explanation may be owing to the stronger musculature in males with more powerful diaphragmatic contractility than in females.

In the present study, ultrasonographic measurements of diaphragmatic thickness and thickening were found to be decreased in patients more than controls. These measurements were highly significantly different among COPD grades of severity with the lowest measurements in patients with very severe COPD. This means that diaphragmatic thickness and thickening were negatively correlated with the severity of COPD.

These results were in agreement with Cohn et al. [21] and Smargiassi et al. [22] who stated that TDTLC mainly was related to the indices of lung hyperinflation, fat-free mass, and BMI. They found that diaphragmatic thickenings were related to the indices of lung hyperinflation (FVC and FEV1), and FEV1/FVC was found to be a determinant of TDTLCRV, which all express the severity of COPD.

This may be explained by airflow limitation resulting in air trapping and lung hyperinflation. Diaphragmatic thicknesses and thickenings express and assess diaphragmatic function, which is defective in COPD.

Lung hyperinflation in moderate to severe COPD puts the inspiratory muscles, particularly the diaphragm, at a significant mechanical disadvantage by shortening its fibers, thereby weakening its force generating capacity. The possible mechanisms of defective diaphragmatic function secondary to hyperinflation could be owing to worsening of the length-tension relationship, decreased length of the zone of apposition, flattening of the diaphragm with decrease in its curvature, change in the mechanical arrangement of costal and crural fibers, and increase in the elastic recoil of the thoracic cage [23].

When end-expiratory lung volume represents ∼70% of predicted total lung capacity, the elastic recoil of the thoracic cage is directed inward so that the inspiratory muscles have to work against the thoracic elastic recoil in addition to intrinsic positive end-expiratory pressure and the elastic recoil of the lungs. The net result is a significant increase in the work of breathing and high oxygen cost in patients with severe COPD [24].

On the contrary, these results were against those of Cimsit et al. [25] who found no correlation between diaphragmatic thickness in patients with COPD and pulmonary function tests except for FEV1% of predicted in patients with mild COPD, and no correlations between diaphragmatic muscle thickness and symptom scores, BMI, or sex.

In the current study, ultrasonography was used to assess diaphragmatic excursion, and no correlation was found between diaphragmatic excursion and sex.

In the present study, diaphragmatic excursion was highly significantly different among patients with COPD with different grades of severity, with the lowest measurements in patients with very severe COPD. This means that excursion was found to correlate negatively with the severity of COPD.

This can be explained by respiratory muscle dysfunction in COPD and decreased capacity of respiratory muscles to meet the increased mechanical load. The diaphragm in COPD is exposed to oxidative stress and sarcomeric injury that increase the proteolytic activity causing wasting of the contractile protein and resulting in loss of force generating capacity of diaphragmatic fibers in COPD [26].

These results were in agreement with Yamaguti et al. [27] who found that diaphragmatic movement (mobility of the right hemidiaphragm assessed by ultrasound by measuring the craniocaudal displacement of the left branch of the portal vein) in patients with COPD was related to indices of lung hyperinflation and was mainly because of air trapping.

These results were against those of Cohn et al. [21] and Smargiassi et al. [22] who found no relation between diaphragmatic excursion and indices of lung hyperinflation and stated that it was only related to BMI.

One of the limitations of this study was the effect of abdominal muscles in the semirecumbent position. This effect could differ resulting in a decrease in the total inspired volume owing to more air trapping and change in end-expiratory lung volume. This bias could influence the relation of ultrasonographic measurements and lung volumes, but this technique was selected to detect the relations of measurements taken under variable circumstances even in patients who could not tolerate the orthostatic position. This technique was slightly different from that reported by Ueki et al. [5] who examined patients in sitting position. These conditions might change the ultrasonographic features of the diaphragm in the zone of apposition and its behavior during contractility, particularly in patients with COPD with hyperinflation. However, this ultrasonographic assessment could estimate lung hyperinflation and evaluate diaphragmatic performance in critically ill patients and those who are mechanically ventilated.


  Conclusion Top


Ultrasonographic measurements of diaphragmatic thickness, thickening, and excursion decrease in COPD, and this decrease is more marked with the progress of the disease, i.e., ultrasound could be a reliable method to assess diaphragmatic function and gives idea about the severity of COPD. Diaphragmatic thickness, thickening, and excursion decrease in female patients more than in males. Both BMI and BODE index are indicators of the severity and progress of COPD.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Puente-Maestu L, Pérez-Parra J, Godoy R, Moreno N, Tejedor A, González-Aragoneses F, et al. Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 2009; 33:1045–1052.  Back to cited text no. 1
    
2.
Sarwal A, Walker FO, Cartwright MS. Neuromuscular ultrasound for evaluation of the diaphragm. Muscle Nerve 2013; 47:319–329.  Back to cited text no. 2
    
3.
Global Initiative for Chronic Obstructive Lung Disease (GOLD). Global strategy for the diagnosis, management and prevention of chronic obstructive pulmonary disease, 2016. Available at: http://www.goldcopd.org. [Last accessed on 2016 Apr 12].  Back to cited text no. 3
    
4.
American Thoracic Society. Lung function testing: selection of reference values and interpretative strategies. Am Rev Respir Dis 1991; 144:202–218.  Back to cited text no. 4
    
5.
Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax 1995; 50:1157–1161.  Back to cited text no. 5
    
6.
Testa A, Soldati G, Giannuzzi R, Berardi S, Portale G, Gentiloni Silveri N, et al. Ultrasound M-mode assessment of diaphragmatic kinetics by anterior transverse scanning in healthy subjects. Ultrasound Med Biol 2011; 37:44–52.  Back to cited text no. 6
    
7.
Hill K, Goldstein RS, Guyatt GH, Blouin M, Tan WC, Davis LL, et al. Prevalence and underdiagnosis of chronic obstructive pulmonary disease among patients at risk in primary care. CMAJ 2010; 182:673–678.  Back to cited text no. 7
    
8.
Yawn B, Mannino D, Littlejohn T, Ruoff G, Emmett A, Raphiou I, et al. Prevalence of COPD among symptomatic patients in a primary care setting. Curr Med Res Opin 2009; 25:2671–2677.  Back to cited text no. 8
    
9.
Sørheim IC, Johannessen A, Gulsvik A, Bakke PS, Silverman EK, DeMeo DL, et al. Gender differences in COPD: are women more susceptible to smoking effects than men? Thorax 2010; 65:480–485.  Back to cited text no. 9
    
10.
Yan Li, Yong-liang Dai, Nan Yu, and You-min Guo. Gender differences of airway dimensions in anatomically matched sites on CT in smokers. COPD 2011; 8:285–292.  Back to cited text no. 10
    
11.
Decramer M, De Benedetto F, Del Ponte A, Marinari S. Systemic effects of COPD. Respir Med 2005; 99:S3–S10.  Back to cited text no. 11
    
12.
Franssen FM, O'Donnell DE, Goossens GH, Blaak EE, Schols AM. Obesity and the lung: obesity and COPD. Thorax 2008; 63:1110–1117.  Back to cited text no. 12
    
13.
Ora J, Laveneziana P, Ofir D, Deesomchok A, Webb KA, O'Donnell DE. Combined effects of obesity and chronic obstructive pulmonary disease on dyspnea and exercise tolerance. Am J Respir Crit Care Med 2009; 180:964–971.  Back to cited text no. 13
    
14.
Zammit C, Liddicoat H, Moonsie I, Makker H. Obesity and respiratory diseases. Int J Gen Med 2010; 3:335–343.  Back to cited text no. 14
    
15.
Guerra S, Sherrill DL, Bobadilla A, Martinez FD, Barbee RA. The relation of body mass index to asthma, chronic bronchitis and emphysema. Chest 2002; 122:1256–1263.  Back to cited text no. 15
    
16.
Sarioglu N, Alpaydin AO, Coskun AS, Celik P, Ozyurt BC, Yorgancioglu A. Relationship between BODE index, quality of life and inflammatory cytokines in COPD patients. Multidiscip Respir Med 2010; 5:84.  Back to cited text no. 16
    
17.
Ong KC, Earnest A, Lu SJ. A multidimensional grading system (BODE index) as predictor of hospitalization for COPD. Chest 2005; 128:3810–3816.  Back to cited text no. 17
    
18.
Celli BR, Cote CG, Marin JM, Casanova C, Montes de Oca M, Mendez RA. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med 2004; 350:1005–10012  Back to cited text no. 18
    
19.
Agusti AG. COPD, a multicomponent disease: implications for management. Respir Med 2005; 99:670–682.  Back to cited text no. 19
    
20.
Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen JA, Boon AJ. Variability in diaphragm motion during normal breathing, assessed with B-Mode ultrasound. J Orthop Sports Phys Ther 2013; 43:927–931.  Back to cited text no. 20
    
21.
Cohn D, Benditt JO, Eveloff S, McCool FD. Diaphragm thickening during inspiration. J Appl Physiol 1997; 83:291–296.  Back to cited text no. 21
    
22.
Smargiassi A, Inchingolo R, Tagliaboschi L, Di Marco Berardino A, Valente S, Corbo GM. Ultrasonographic assessment of the diaphragm in chronic obstructive pulmonary disease patients: relationships with pulmonary function and the influence of body composition – a pilot study. Respiration 2014; 87:364–371.  Back to cited text no. 22
    
23.
De Troyer A, Wilson TA. Effect of acute inflation on the mechanics of the inspiratory muscles. J Appl Physiol Bethesda Md 2009; 107:315–323.  Back to cited text no. 23
    
24.
O'Donnell DE, Webb KA, Neder JA. Lung hyperinflation in COPD: applying physiology to clinical practice. COPD Res Pract 2015; 1:4.  Back to cited text no. 24
    
25.
Cimsit C, Bekir M, Karakurt S, Eryuksel E. Ultrasound assessment of diaphragm thickness in COPD. Marmara Med J 2016; 29:8–13.  Back to cited text no. 25
    
26.
Ottenheijm CAC, Heunks LMA, Dekhuijzen RPN. Diaphragm adaptations in patients with COPD. Respir Res 2008; 9:12.  Back to cited text no. 26
    
27.
Dos Santos Yamaguti WP, Paulin E, Shibao S, Chammas MC, Salge JM, Ribeiro M. Air trapping the major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients. Respirology 2008; 13:138–144.  Back to cited text no. 27
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Patients and Methods
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed205    
    Printed8    
    Emailed0    
    PDF Downloaded21    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]