|Year : 2019 | Volume
| Issue : 4 | Page : 459-468
Correlation between ventricular function as assessed by echocardiography and six-minute walk test as a surrogate of functional capacity in patients with chronic obstructive pulmonary disease
Magdy M Khalil1, Hala M Salem1, Hossam-Eldin M Abdil-Hamid1, Muhammad Y Zakaria2
1 Department of Chest Diseases, Faculty of Medicine, Ain Shams University, Cairo, Egypt
2 Respiratory ICU Department, Kafr El-Sheikh Chest Hospital, Ministry of Health, Kafr El-Sheikh, Egypt
|Date of Submission||29-May-2019|
|Date of Decision||06-Aug-2019|
|Date of Acceptance||09-Sep-2019|
|Date of Web Publication||25-Oct-2019|
MSc Muhammad Y Zakaria
Borg El-Burrulos, Kafr El-Sheikh
Source of Support: None, Conflict of Interest: None
Background Exercise intolerance is common in patients with chronic obstructive pulmonary disease (COPD), which has multiple mechanisms underlying its progression. Ventricular dysfunction may play a role in the development of exercise incapacity in patients with COPD.
Aim To investigate the possible contribution of left ventricular (LV) and right ventricular (RV) dysfunction (either systolic or diastolic) in development of exercise intolerance in patients with COPD.
Patients and methods A total of 60 patients with diagnosis of COPD were categorized according to GOLD spirometric stage into two groups (group 1: mild to moderate COPD, and group 2: severe to very severe COPD). Both groups were evaluated by spirometry, ECG, chest radiography, routine laboratory investigation, 6-min walk test, and echocardiography including tissue Doppler imaging.
Results The average age in the whole study group was 56.63±10.33 years. Male patients in the study were 46 (76.7%) and female patients were 14 (23.3%). Mean maximum walk distance among the whole group was 342.75±54.85 m. There was a significant correlation between 6-min walk distance and transtricuspid E velocity, tricuspid E/A, and transtricuspid deceleration time (P=0.011, 0.015, and 0.021, respectively). There was no significant correlation between 6-min walk distance and parameters of LV diastolic dysfunction. Prevalence of ventricular dysfunction was as follow: LV systolic dysfunction 3.3%, LV diastolic dysfunction 30%, RV systolic dysfunction 21%, and RV diastolic dysfunction 46%.
Conclusion RV diastolic dysfunction may be a contributing factor in the progression of exercise intolerance in COPD. Although LV diastolic dysfunction may not be associated with exercise intolerance, it is still prevalent in COPD and must be assessed and managed through the course of the disease and especially during exacerbation.
Keywords: 6-min walk test, chronic obstructive pulmonary disease, echocardiography, exercise intolerance, ventricular dysfunction
|How to cite this article:|
Khalil MM, Salem HM, Abdil-Hamid HEM, Zakaria MY. Correlation between ventricular function as assessed by echocardiography and six-minute walk test as a surrogate of functional capacity in patients with chronic obstructive pulmonary disease. Egypt J Bronchol 2019;13:459-68
|How to cite this URL:|
Khalil MM, Salem HM, Abdil-Hamid HEM, Zakaria MY. Correlation between ventricular function as assessed by echocardiography and six-minute walk test as a surrogate of functional capacity in patients with chronic obstructive pulmonary disease. Egypt J Bronchol [serial online] 2019 [cited 2019 Nov 20];13:459-68. Available from: http://www.ejbronchology.eg.net/text.asp?2019/13/4/459/269684
| Introduction|| |
Chronic obstructive pulmonary disease (COPD) is on its way to be the third most common killer disease worldwide by 2020 ,. Although being of primary pulmonary origin, it has a unique physiological and pathophysiological characteristics that may cause extrapulmonary effects and comorbidities ,,. Comorbidities are associated with high mortality, reduced compliance to medications, and diminished quality of life . Cardiovascular comorbidities are among the most frequently seen comorbidities associated with COPD ,. Many studies have demonstrated a strong association between heart failure and COPD ,,.
Exercise intolerance is common in patients with COPD, which has multiple mechanisms underlying its progression. Increased ventilatory demand, associated with altered dynamic mechanics, abnormal gas exchange, airway limitation, and peripheral muscle dysfunction, is among the intrinsic pulmonary mechanisms that are alleged for exercise incapacity seen in such patients ,,,,. There is increasing evidence that ventricular dysfunction may play a role in development of exercise intolerance in patients with COPD.
In the present study, we tried to assess the left ventricular (LV) and right ventricular (RV) function either systolic or diastolic in patients with COPD. We tried to correlate echocardiographic parameters of ventricular function with 6-min walk test as a surrogate for exercise capacity to reveal any contribution of ventricular function on exercise intolerance found in patients with COPD.
| Patients and methods|| |
The protocol of the study was approved by Research Ethics Committee REC, Ain Shams University (FMASU MD 196/2016). The study included 60 patients. Inclusion criteria entailed sure diagnosis of COPD (presence of risk factors, clinical symptoms and signs, radiology, and spirometry) among patients who were admitted to inpatient and outpatient clinic in Kafr El-Sheikh Chest Hospital in the period from December 2016 to July 2018. Exclusion criteria were the presence of severe liver or kidney disease, presence of recent or old ischemic heart disease or other valvular heart disease, severe systemic hypertension, pulmonary disease other than COPD, acute venous thromboembolism, hemoglobin less than 10 g/dl, patients who cannot perform spirometry or 6-min walk test, and patients with acute exacerbation of COPD. After taking a written and informed consent from all patients participating in the study, patients were categorized according to GOLD spirometric criteria into group 1 (mild to moderate COPD, forced expiratory volume in 1 s (FEV1)/forced vital capacity <70%, and FEV1>50%) and group 2 (severe to very severe COPD, FEV1/forced vital capacity <70%, and FEV1<50%). Routine laboratory investigations to exclude severe liver or kidney diseases were performed. Chest radiography to ensure hyperinflation and rule out any other chest diseases and ECG to exclude ischemic changes or arrhythmias were done. Six-min walk test was performed according to ATS guidelines for all participants . Patients were instructed to walk through a corridor of 30-m length as fast as they can for 6 min. They were encouraged by simple words throughout the test and were instructed to stop immediately if they feel they cannot complete the test or if any complications occurred. The outcome of the test was recorded as the maximum distance the patient walked, the basal and post-test heart rate, the basal and post-test oxygen saturation, and complication during the test (if occurred). Echocardiography was done for all patients in the cardiology department, EL-Obour Insurance Hospital, using General Electric (GE) machine, VIVID S5, with a transducer (probe), 3S-RS 1.5–3.6 MHz. Images were acquired according to the latest guidelines , ([Figure 1]) and revised by two cardiologists in the department.
|Figure 1 (a) Linear dimensions of right ventricle: basal diameter, mid cavity, and longitudinal. (b) TAPSE by applying M-mode at the lateral free wall of RV. (c) Myocardium velocities by TDI at the lateral tricuspid annulus: 1→ S’, 2→ E’. (d) Transmitral flow parameters: E, A, and E/A. RV, right ventricular; TAPSE, tricuspid annular plane excursion; TDI, tissue Doppler imaging.|
Click here to view
Linear LV dimension was taken from parasternal long-axis PLAX at the end of diastole, and ejection fraction (by Teicholtz method) and fractional shortening were derived. Transmitral flow was assessed using E, A, E/A, and deceleration time. Then tissue Doppler imaging (TDI) modality was used to measure e’, and E/e’ was calculated.
RV linear dimensions were obtained in apical four-chamber view. Tricuspid annular plane excursion (TAPSE) was measured by 2D modality, and then transtricuspid flow was assessed similar to transmitral flow using E, A, E/A, and deceleration time. TDI was used to measure myocardial peak tricuspid annular velocity (S’) and E’, and then E/E’ was calculated.
LV systolic dysfunction was present when EF is less than 50%. LV diastolic dysfunction was present when two of the following criteria are present : (a) lateral e’ velocity less than 10 m/s (0.10 m/s), (b) E/e’ more than 14, and (c) tricuspid regurgitant velocity more than 2.8 m/s.
RV systolic dysfunction was present when TAPSE less than 1.6 cm or S’ less than 10 cm/s (0.10 m/s). RV diastolic dysfunction was present when one of the following was present: (a) E/A<0.8, (b) E/A from 0.8 to 2.1 and E/E’ >6, and (c) E/A more than 2.1 and deceleration time less than 120 ms.
The collected data were revised, coded, tabulated, and introduced to a PC using Statistical package for Social Science (SPSS 25; IBM SPSS version 25, Chicago, Illinois, USA). Data were presented, and suitable analysis was done according to the type of data obtained for each parameter. Student t test and Mann–Whitney test (U test) were used to assess the statistical significance of the difference of parametric and nonparametric variables (respectively) between two study groups. χ2 test and Fisher’s exact test were used to examine the relationship between two qualitative variables according to their number. Correlation analysis (using Pearson’s method) was used to assess the strength of association between two quantitative variables.
| Results|| |
[Table 1] summarizes patients data, comorbidities, laboratory investigations, arterial blood gases, spirometry, and 6-min walk test. Male patients in the study were 46 (76.7%) and female patients were 14 (23.3%). Both groups included 23 (76.67%) males and seven (23.33%) females. Dyspnea was the most frequent complaint. Most patients were current smokers (46.7%) or ex-smokers (30.0%). Systemic arterial hypertension was the most common comorbidity (21%). One patient had hypothyroidism and liver cirrhosis, and an another one had hypertension and HCV. Normal sinus rhythm with no ischemia was the most common finding in ECG, and all patients showed signs of hyperinflated chest on plain chest radiography. Mean±SD maximum walk distance among the whole group was 342.75±54.85 m, mean±SD maximum walk distance was 373.33±41.86 m in group A and 312.17±49.32 m in group B. Mean LV and RV echocardiographic parameters representative of both systolic and diastolic functions are summarized in [Table 2].
|Table 1 Patients data, laboratory investigations, arterial blood gas, pulmonary function test, and 6-min walk test results|
Click here to view
|Table 2 Echocardiographic parameters of left and right systolic and diastolic functions|
Click here to view
Correlation between 6-min walk test and ventricular function
There was a significant positive correlation between 6-min walk distance and ejection fraction of the LV among the whole study group. There was no significant correlation between 6-min walk distance and other parameters of LV diastolic dysfunction. Regarding the RV, there was a significant correlation between 6-min walk distance and transtricuspid E velocity ([Figure 2]), tricuspid E/A ([Figure 3]), and transtricuspid deceleration time ([Figure 4]) (P=0.011, 0.015, and 0.021, respectively). These are parameters of RV diastolic dysfunction. There was a significant correlation between 6-min walk distance and TAPSE (parameter indicative of systolic function) in mild to moderate COPD. In patients with severe to very severe COPD, there was a significant correlation between 6-min walk distance and RV E/A ([Figure 5]).
|Figure 2 Correlation between 6-min walk distance and RV transtricuspid E velocity. A lower 6-min walk distance is associated with lower E velocity among the whole study group. RV, right ventricular.|
Click here to view
|Figure 3 Correlation between 6-min walk distance and right ventricular E/A in the whole study group. A lower 6-min walk distance is associated with lower E/A ratio.|
Click here to view
|Figure 4 Correlation between 6-min walk distance and right ventricular deceleration time in the whole study group. A lower 6-min walk distance is associated with lower deceleration time.|
Click here to view
|Figure 5 Correlation between 6-min walk distance and transtricuspid E/A in group B. A lower 6-min walk distance is correlated with a lower E/A in patients with severe to very severe COPD. COPD, chronic obstructive pulmonary disease.|
Click here to view
Prevalence of ventricular systolic and diastolic dysfunction in patients with chronic obstructive pulmonary disease
LV systolic dysfunction was present in 3.3% of study population ([Table 3]). There was no significant difference between both groups. LV diastolic dysfunction occurred in 18 (30%) patients. Among these 18 patients, grade 1 diastolic dysfunction (impaired relaxation) was present in 15 (25%) patients and grade 2 diastolic dysfunction (pseudonormal filling) was present in three (5%) patients.
RV systolic dysfunction occurred in 13 (21.7%) patients. There was no significant difference between both groups. RV diastolic dysfunction occurred in 28 (46.7%) patients. Among these 28 patients, grade 1 diastolic dysfunction (impaired relaxation) was present in 14 (23.3%) patients, grade 2 diastolic dysfunction (psuedonormal filling) was present in 11 (18.3%) patients and grade 3 diastolic dysfunction (restrictive filling) was present in three (5%) patients. There was a significant difference between both groups, with an increased prevalence of diastolic dysfunction among severe and very severe COPD. Prevalence of RV diastolic dysfunction in this group reached 76%, which supports the accumulating evidence of the importance of RV pathology in the course of the disease.
| Discussion|| |
The main findings in the present study are the high prevalence of RV and LV diastolic dysfunction in patients with COPD, and the presence of significant correlation between RV diastolic dysfunction and 6-min walk test, implying a contribution of RV diastolic dysfunction on exercise incapacity.
In the present study, we found no significant correlation between 6-min walk distance and other parameters of LV diastolic dysfunction. In contrast with our study, López-Sánchez et al.  found a significant correlation between decreased 6-min walk distance and E/A, indicating contribution of LV diastolic dysfunction in patients’ exercise intolerance. One of the limitations of their study is the exclusion of mild to moderate COPD and very severe COPD. They only included patients with severe COPD, which may explain this difference in results. Fenster et al.  did not found this association between LV diastolic dysfunction and 6-min walk distance reported by López-Sánchez et al.. Another study by Schoos et al.  did not find a correlation between LV diastolic dysfunction and 6-min walk distance. Another recent study by Muller et al.  compared patients with COPD having LV diastolic dysfunction with patients having no diastolic dysfunction using cardiopulmonary exercise test. They found no association between LV diastolic dysfunction and worsening of exercise tolerance.
Watz et al.  estimated Pro-BNP as a marker of myocardial failure and correlated it with 6-min walk test. They concluded that physical activity is associated with LV diastolic dysfunction. Pro-BNP is not specific for LV pathologies and may be increased in RV dysfunction. Patients with LV dysfunction may also have RV dysfunction, which causes the observed exercise intolerance.
Regarding the RV, there was a significant correlation between 6-min walk distance and parameters of RV diastolic dysfunction. This positive correlation among the whole study group suggests a decreased exercise capacity in presence of RV diastolic dysfunction irrespective of COPD spirometric stage, which may suggest that even in mild and moderate airflow limitation, when RV diastolic dysfunction develops, exercise incapacity may evolve.
The role of ventricular dysfunction in progression of exercise intolerance in COPD was not fully determined. Furthermore, the RV was always neglected in traditional workup and studies to the extent that it was once coined as ‘the forgotten chamber’ . The present study supports the results of Fenster et al. , who studied the correlation between 6-min walk test and RV diastolic function. They found a positive significant correlation between 6-min walk distance and RV E/A. They concluded that RV diastolic dysfunction may contribute to exercise intolerance in patients with COPD . They referred the association between RV diastolic dysfunction and decreased exercise tolerance to diminished RV preload and stroke volume, which may be exacerbated during exercise . Although Schoos et al.  did not find this association between lower 6-min walk distance and RV diastolic dysfunction, they reported a reduction in RV diastolic function parameters. In addition, they excluded mild COPD and very severe COPD, which may affect the overall correlation. Cuttica et al. , in their study of patients without severely impaired lung function, demonstrated that structural changes of the right heart are associated with a decrement in 6-min walk distance independent of spirometric stage. However, they did not find an association between 6-min walk distance and RV systolic function as assessed by TAPSE or LV systolic or diastolic function .
Although our study did not include control group, there is a large body of evidence that LV dysfunction is prevalent in patients with COPD ,,,,,. Prevalence of LV diastolic dysfunction varies largely between different studies. Our estimate is relatively close to another study by Gupta et al.  who reported a prevalence of 47.5% among their study group which include 40 patients with COPD of different spirometric stages. Another recent study by Jatav et al.  estimated LV diastolic dysfunction to be 46% in a sample of 100 patients with COPD. This is in contrary to a study performed by Miranda et al.  who reported a prevalence of LV diastolic dysfunction of 88% among their study group and also observed a significant difference between both groups of study (group 1: mild to moderate COPD and group 2: severe to very severe COPD). López-Sánchez et al.  found LV diastolic dysfunction in 90% of their group (80% grade 1 and 10% grade 2). Rawy and Fathalla  reported a prevalence of 73.3%. However, many authors argue that, Freixa et al. reported a prevalence of 12% in COPD patients on their first hospital admissions . But actually Freixa and colleagues found diastolic dysfunction in about 60% of their study sample but were exposed to error in data summarization and reporting.
This difference in the prevalence of diastolic dysfunction may be owing to variability in echocardiographic parameters needed to diagnose and grade diastolic dysfunction. One of the contributions of the present study is the utilization of the most recent algorism suggested by the American Society of Echocardiography published in 2016 for diagnosis and grading of LV diastolic dysfunction in our patients’ diagnosis and grading. Systemic hypertension and cardiac ischemia are the most common causes of diastolic dysfunction. Another contribution of the present study is the exclusion of patients with a prior history of ischemic heart diseases, and patients with severe arterial hypertension who may not be excluded in some other studies .
In the present study, RV systolic dysfunction occurred in 13 (21.7%) patients. There was no significant difference between both groups. In the previously mentioned study by Jatav et al. , RV systolic dysfunction was present in 14% of patients. In the study by Gupta et al. , RV systolic dysfunction was present in 7.5% of patients. In their study, RV systolic dysfunction was diagnosed by eyeballing when observing wall motion hypokinesia. Obviously, this method may underestimate the presence of impaired function in many patients. Vizza et al.  estimated the prevalence of RV systolic dysfunction (defined by RV ejection fraction <45%) in patients with COPD as 59%. An advantage of using TDI to assess RV function is that measurement is independent of geometric assumptions and endocardial border tracing. Another strength of the present study is the incorporation of TDI parameters like peak tricuspid lateral annulus velocity (S’) in assessment of RV systolic function evaluation.
Importantly, RV dysfunction either systolic or diastolic was formerly linked to development of pulmonary hypertension. The increased pulmonary vascular resistance with subsequent increase in RV afterload will lead to RV hypertrophy, and then dilation and even RV failure. Recent studies have demonstrated that RV dysfunction may occur even in the absence of pulmonary hypertension. They referred RV changes to other mechanisms such as systemic inflammation, microvascular ischemia, hypoxia, systemic hypertension and obesity ,,,,,. Hilde et al.  concluded a similar observation about the presence of RV function changes in absence of pulmonary hypertension in patients with COPD.From a clinical point of view, exercise training is proved to enhance exercise capacity and quality of life in patients with heart failure with preserved ejection fraction , which is frequently caused by RV dysfunction ,,, or LV diastolic dysfunction . Owing to the high prevalence of RV systolic and diastolic dysfunction and LV diastolic dysfunction in our patients with COPD, exercise training should be prescribed in patients with COPD having these ventricular abnormalities. Moreover, avoiding tachycardia by correcting hypoxemia and optimizing medication is mandatory to maintain LV filling . It is not clear whether phosphodiesterase inhibitors (PDE 5) − which is proved to improve RV function  − enhance RV function by direct mechanism or by improving RV afterload . So, the role of PDE 5 in RV diastolic dysfunction in patients with COPD should be evaluated. Again, LV diastolic dysfunction and RV dysfunction should be assessed and managed promptly in every COPD exacerbation as they may be the cause of cardiac decompensation responsible for this exacerbation .
The study was cross-sectional, so firm conclusions about causality cannot be made. Moreover, we did not have a control group, so we used reference values from literature. Performing echocardiography was difficult in patients with COPD because of the limited acoustic window owing to hyperinflation; however, only measurements with a satisfactory image quality have been used for analyses.
In conclusion, RV diastolic dysfunction may be a contributing factor in progression of exercise intolerance in COPD regardless of patients’ spirometric stage. Although LV diastolic dysfunction may not be associated with exercise intolerance, it is still prevalent in COPD and must be assessed and managed through the course of the disease and especially during exacerbation.
The authors thank professor Muhammad Kamal Salama, MD, professor of cardiology, Aswan University, for his great help and consultation in this study. The authors also thank their colleagues, Dr Mahmoud Nasr, Dr Emad El-Gammal, Dr Hamada Abdul-Baset, and Dr Asmaa Barakat, cardiologists in Cardiology Department, El-Obour Hospital, for their great help and assistance in performing echocardiography for their patients. Moreover, the authors thank Dr Eslam Saboukh, a lecturer of cardiology, Kafr El-Sheikh University, for his great help and advice.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V et al.
Global and regional mortality from 235 causes of death for 20 age groups in1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet
Yin H, Yin S, Lin Q, Xu Y, Xu H, Liu T. Prevalence of comorbidities in chronic obstructive pulmonary disease patients: a meta-analysis. Medicine
Brown JP, Martinez CH. Chronic obstructive pulmonary disease comorbidities. Curr Opin Pulm Med
Chatila WM, Thomashow BM, Minai OA, Criner GJ, Make BJ. Comorbidities in chronic obstructive pulmonary disease. Proc Am Thorac Soc
Hillas G, Perlikos F, Tsiligianni I, Tzanakis N. Managing comorbidities in COPD. Int J Chron Obstruct Pulmon Dis
Huiart L, Ernst P, Suissa S. Cardiovascular Morbidity and Mortality in COPD. Chest
Chetty U, Mclean G, Morrison D, Agur K, Guthrie B. Chronic obstructive pulmonary disease and comorbidities: a large cross-sectional study in primary care. Br J Gen Pract
De Miguel DJ, García TG, Maestu LP. Comorbidities in COPD. Arch Bronconeumol
Cavaille A, Gut-gobert C, Marchand-adam S, Meurice J, Morel H, Person-tacnet C. Comorbidities of COPD. Eur Respir Rev
O’Donnell DE, Elbehairy AF, Domnik NJ, Vincent S, Guenette JA, Webb KA et al.
Patterns of cardiopulmonary response to exercise in COPD. In Palange P, Laveneziana P, Neder JA et al.
, editors. Clinical exercise testing (ERS monograph)
. Sheffield: European Respiratory Society; 2018. 107.
O’donnell DE, D’arsigny C, Fitzpatrick M, Webb KA. Exercise hypercapnia in advanced chronic obstructive pulmonary disease: the role of lung hyperinflation. Am J Respir Crit Care Med
Marin JM, Carrizo SJ, Gascon M, Sanchez A, Gallego B, Celli BR. Inspiratory capacity, dynamic hyperinflation, breathlessness, and exercise performance during the 6-minute-walk test in chronic obstructive pulmonary disease. Am J Respir Crit Care Med
Caviedes IR, Delgado I, Soto R. Ventilatory inefficiency as a limiting factor for exercise in patients with COPD. Respir Care
Gosselink R, Troosters T, Decramer M. Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med
Crapo RO, Casaburi R, Coates AL, Enright PL, MaCintyre NR, Mckay RT et al.
ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med
Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K et al.
Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr
Lang RM, Badano LP, Mor-avi V, Afilalo J, Armstrong A, Ernande L et al.
Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr
Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, Dokainish H, Edvardsen T et al.
Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur J Echocardiogr
López-Sánchez M, Muñoz-esquerre M, Huertas D, Gonzalez-costello J, Manresa F, Dorca J et al.
High prevalence of left ventricle diastolic dysfunction in severe copd associated with a low exercise capacity: a cross-sectional study. PloS One
Fenster BE, Holm KE, Weinberger HD, Moreau KL, Meschede K, Crapo JD et al.
Right ventricular diastolic function and exercise capacity in COPD. Respir Med
Schoos MM, Dalsgaard M, Kjærgaard J, Moesby D, Jensen SG, Steffensen I et al.
Echocardiographic predictors of exercise capacity and mortality in chronic obstructive pulmonary disease. BMC Cardiovasc Disord
Muller PT, Utida KAM, Augusto TRL, Spreafico MVP, Mustafa RC, Xavier AW et al.
Left ventricular diastolic dysfunction and exertional ventilatory inefficiency in COPD. Respir Med
Watz H, Waschki B, Boehme C, Claussen M, Meyer T, Magnussen H. Extrapulmonary Effects of chronic obstructive pulmonary disease on physical activity a cross-sectional study. Am J Respir Crit Care Med
Rigolin VH, Robiolio PA, Wilson JS, Harrison JK, Bashore TM. The forgotten chamber: the importance of the right ventricle. Cathet Cardiovasc Diagn
Cuttica MJ, Shah SJ, Rosenberg SR, Orr R, Beussink L, Jane E et al.
Right heart structural changes are independently associated with exercise capacity in non-severe COPD. PLoS One
Gupta NK, Agrawal RK, Srivastav AB, Ved ML. Echocardiographic evaluation of heart in chronic obstructive pulmonary disease patient and its co-relation with the severity of disease. Lung India
Jatav VS, Meena SR, Jelia S, Jain P, Ajmera D, Agarwal V et al.
Echocardiographic findings in chronic obstructive pulmonary disease and correlation of right ventricular dysfunction with disease severity. IJAM
Miranda L, Caram DO, Ferrari R, Naves CR, Tanni SE, Sousa L et al.
Association between left ventricular diastolic dysfunction and severity of chronic obstructive pulmonary disease. Clinics
Rawy AM, Fathalla D. Left ventricular diastolic dysfunction in patients with chronic obstructive pulmonary disease (COPD), prevalence and association with disease severity: Using tissue Doppler study. Egypt J Chest Dis Tuberc
Freixa X, Portillo K, Paré C, Garcia-Aymerich J, Gomez FP, Benet M et al.
Echocardiographic abnormalities in patients with COPD at their first hospital admission. Eur Respir J
Vizza CD, Lynch JP, Ochoa LL, Richardson G, Trulock EP. Right and left ventricular dysfunction in patients with severe pulmonary disease. Chest
Huez S, Faoro V, Guénard H, Martinot JB, Naeije R. Echocardiographic and tissue Doppler imaging of cardiac adaptation to high altitude in native highlanders versus acclimatized lowlanders. Am J Cardiol
Huez S, Roufosse F, Vachiéry JL, Pavelescu A, Derumeaux G, Wautrecht JC et al.
Isolated right ventricular dysfunction in systemic sclerosis: latent pulmonary hypertension? Eur Respir J
Cicala S, Galderisi M, Caso P, Petrocelli A, D’Errico A, De Divitiis O et al.
Right ventricular diastolic dysfunction in arterial systemic hypertension: analysis by pulsed tissue Doppler. Eur J Echocardiogr
Rawat DK, Alzoubi A, Gupte R, Chettimada S, Watanabe M, Kahn AG et al.
Increased reactive oxygen species, metabolic maladaptation, and autophagy contribute to pulmonary arterial hypertension-induced ventricular hypertrophy and diastolic heart failure. Hypertension
Zhuiko A, Gertcen M, Atroschenko E. Right ventricular diastolic function in patients with COPD and heart failure, depending on endothelial function. Eur Respir J
Hilde JM, Skjørten I, Grøtta J, Hansteen V, Melsom MN, Hisdal J et al.
Right ventricular dysfunction and remodeling in chronic obstructive pulmonary disease without pulmonary hypertension. J Am Coll Cardiol
Kitzman DW, Brubaker PH, Herrington DM, Morgan TM, Stewart KP, Hundley WG et al.
Effect of endurance exercise training on endothelial function and arterial stiffness in older patients with heart failure and preserved ejection fraction: a randomized, controlled, single-blind trial. J Am Coll Cardiol
Edelmann F, Gelbrich G, Düngen HD, Fröhling S, Wachter R, Stahrenberg R et al.
Exercise training improves exercise capacity and diastolic function in patients with heart failure with preserved ejection fraction: results of the Ex-DHF (Exercise training in Diastolic Heart Failure) pilot study. J Am Coll Cardiol
Melenovsky V, Hwang SJ, Lin G, Redfield MM, Borlaug BA. Right heart dysfunction in heart failure with preserved ejection fraction. Eur Heart J
Mohammed SF, Hussain I, AbouEzzeddine OF, Takahama H, Kwon SH, Forfia P et al.
Right ventricular function in heart failure with preserved ejection fraction: a community-based study. Circulation
Gorter TM, Hoendermis ES, van Veldhuisen DJ, Voors AA, Lam CSP, Geelhoed B et al.
Right ventricular dysfunction in heart failure with preserved ejection fraction: a systematic review and meta‐analysis. Eur J Heart Fail
Puwanant S, Priester TC, Mookadam F, Bruce CJ, Redfield MM, Chandrasekaran K. Right ventricular function in patients with preserved and reduced ejection fraction heart failure. Eur J Echocardiogr
Kane GC, Karon BL, Mahoney DW, Redfield MM, Roger VL, Burnett JC et al.
Progression of left ventricular diastolic dysfunction and risk of heart failure. JAMA
Boussuges A, Pinet C, Molenat F, Burnet H, Ambrosi P, Badier M et al.
Left atrial and ventricular filling in chronic obstructive pulmonary disease an echocardiographic and Doppler study. Am J Respir Crit Care Med
Gan CTJ, Holverda S, Marcus JT, Paulus WJ, Marques KM, Bronzwaer JGF et al.
Right ventricular diastolic dysfunction and the acute effects of sildenafil in pulmonary hypertension patients. Chest
Abusaid GH, Barbagelata A, Tuero E, Mahmood A, Sharma G. Diastolic dysfunction and COPD exacerbation. Postgrad Med
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]