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(Chest. 2000;118:1063-1068.)
© 2000 American College of Chest Physicians

Right Ventricular Dysfunction in Adult Severe Cystic Fibrosis*

Viorel G. Florea, MD, PhD{dagger}; Natalia D. Florea, MD; Rakesh Sharma, BSc; Andrew J. S. Coats, DM; Derek G. Gibson, MD; Margaret E. Hodson, MD and Michael Y. Henein, MD, PhD

* From the Department of Cardiac Medicine (Drs. V.G. Florea, N.D. Florea, Coats, Gibson, and Henein and Mr. Sharma), National Heart and Lung Institute, London, UK; and the Department of Cystic Fibrosis (Dr. Hodson), Royal Brompton Hospital, London, UK. {dagger} Currently at Department of Medicine, University of Minnesota Medical School and VA Medical Center, Minneapolis, MN.

Correspondence to: Michael Y. Henein, MD, PhD, Department of Cardiac Medicine, National Heart and Lung Institute, London, SW3 6LY, UK; e-mail: m.henein{at}rbh.nthames.nhs.uk


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: This study sought to assess the extent of impairment of cardiac function in adult patients with end-stage cystic fibrosis (CF) and to examine the relationship between cardiovascular abnormalities and the degree of hypoxemia and hypercapnia.

Design and setting: A retrospective study in a tertiary cardiac and CF center.

Participants and interventions: A total of 103 adult patients with end-stage CF awaiting lung or heart and lung transplantation (mean age [± SD], 26 ± 7 years; 54 men) underwent Doppler echocardiography and arterial blood gas analysis (mean PaO2, 54 ± 10 mm Hg; mean PaCO2, 47 ± 8 mm Hg). The findings were compared to those of 17 healthy control subjects (mean age, 24 ± 7 years; 13 men) who had no history of cardiac or pulmonary disease.

Measurements and results: All patients were in sinus rhythm with a mean tachycardia of 112 ± 18 beats/min (control subjects, 76 ± 16; p < 0.0001) and had a cardiac output of 5.3 L/min (control subjects, 4.3 L/min; p < 0.04). In the patient group, the left ventricular (LV) dimensions, systolic and diastolic function, and wall thickness were all within normal limits. The mean amplitude of long-axis excursion in patients was normal at the LV site, but that of the right ventricular (RV) free wall was significantly reduced as compared with control subjects (1.6 ± 0.4 vs 2.2 ± 0.4 cm, respectively; p < 0.001), which was found to correlate with the degree of hypoxemia (r = 0.63; p < 0.02) and hypercapnia (r = -0.68; p < 0.01). RV diastolic function, which was represented by the relative isovolumic relaxation time to cardiac cycle length, was longer in patients than in control subjects (8.7 ± 4.8% vs 5.0 ± 3.0%, respectively; p < 0.03). The pulmonary flow acceleration time (90 ± 22 vs 121 ± 34 ms, respectively; p < 0.01) and the systolic stroke distance (7.0 ± 2.2 vs 10.5 ± 1.9 cm/s2; p < 0.001) were both lower than normal.

Conclusions: This study confirms the presence of significant RV systolic and diastolic dysfunction in the setting of consistent tachycardia and increased cardiac output in adult CF patients with severe disease. No specific LV abnormalities were detected in these patients.

Key Words: cystic fibrosis • echocardiography • right ventricular function


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Cystic fibrosis (CF), the most common life-threatening autosomal recessive disorder in the white population,1 is caused by mutations in the CF trans- membrane conductance regulator gene on chromosome 72 and occurs at a frequency of approximately 1:2,000 to 1:2,500 live births.3 Advances in medical therapy have resulted in an improvement in prognosis and quality of life with increasing numbers of patients surviving into adult life.4 5 As the disease progresses, patients develop disabling lung disease with cardiovascular involvement, some eventually developing overt cor pulmonale.6 Although clinically apparent cor pulmonale is a preterminal event in some patients with CF, the prevalence of subclinical cardiac dysfunction remains unclear.

Although hypoxemia has been well-documented in patients with CF,7 8 9 the role of hypoxemia and hypercapnia in the development of right ventricular (RV) dysfunction has not been demonstrated conclusively. The proportion of patients with CF who have cardiac involvement differs widely between studies, ranging from 0 to 100% for RV dysfunction10 11 12 13 and 0 to 33% for left ventricular (LV) dysfunction.11 12 13 All of these studies however, have been carried out on relatively small and heterogeneous populations. The present study addresses this issue in a larger population of patients. The study was undertaken in order to assess the extent of impairment of cardiac function in adult patients with CF and to examine the relationship between cardiovascular abnormalities and the degree of hypoxemia and hypercapnia in 103 adult patients with end-stage CF who were awaiting lung or heart and lung transplantation.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
The target population for this study comprised patients with CF who were referred for echocardiography as part of their transplant assessment at the Royal Brompton Hospital between March 1989 and March 1999. Standard criteria were used when referring patients to the bilateral single lung/heart-lung transplant waiting list.14 A total of 103 consecutive patients were studied. Two patients were excluded due to incomplete data. The diagnosis of CF was based on positive sweat tests with typical clinical findings, with or without genotype confirmation. The age range for the patients was between 15 and 57 years (mean [± SD] age, 26 ± 7 years), of whom 54 were men. Of the 103 patients recruited into this study, 7 patients had clinical evidence of overt right-sided heart failure, which was treated with diuretics. All patients had chronic respiratory infections, but none of them were having an acute exacerbation at the time of the study. The choice between lung vs heart-lung transplantation was not based on the severity of cardiac dysfunction but, rather, on the availability of donor organs.

In addition, 17 healthy control subjects (mean age, 24 ± 7 years; 13 men) were recruited. None of the control subjects had any clinical evidence of cardiac or pulmonary disease.

Procedures
Simultaneous Doppler echocardiograms and phonocardiograms were recorded along with standard lead II of the ECG with the patient supine and in the left semilateral position. All patients were studied at rest and in quiet respiration on room air.

Echocardiograms were recorded using an echocardiograph (Sonos 1500; Hewlett-Packard; Palo Alto, CA) with a 2.5-MHz imaging transducer. Standard LV size and function were assessed from left parasternal, apical, and subcostal views. LV systolic and diastolic dimensions, septal thickness, and posterior wall thickness were measured from the M-mode recordings of the LV minor axis using leading edge methodology. LV long-axis recordings were obtained from the apical four-chamber view, with the transducer at the apex and the M-mode cursor at the left, and septal sites of the mitral ring and RV long axis from the free wall of the tricuspid ring.15 Blood flow velocities were recorded by pulsed Doppler echocardiography; pulmonary forward flow velocities were measured from the parasternal short-axis view with the sample volume at the valve level and were adjusted until an optimal trace was obtained with maximum acoustic energy in the envelope. Transmitral and transtricuspid forward flow velocities were obtained in the same way from the apical four-chamber view with the sample volume by the tips of mitral and tricuspid valve leaflets, respectively. All traces were recorded photographically at a paper speed of 100 mm/s. Mitral and tricuspid regurgitation were detected by color flow Doppler and registered using continuous-wave Doppler across the two valves, respectively.

Phonocardiograms were recorded (Cambridge Instrument Company; Cambridge, UK) from the right or left sternal edge in the position where A2 was most obvious. The identity of A2 itself was checked against the aortic valve closure artifact on pulsed Doppler, and its timing was taken as that of the onset of the first high-frequency component.

Measurements
LV end-diastolic dimensions (LVEDDs) were taken at the onset of the q wave of the simultaneously recorded ECG, and LV end-systolic dimensions (LVESDs) were measured at the first high-frequency aortic component of the second heart sound (A2) on the phonocardiogram. LV fractional shortening was calculated as the percentage of the fall in dimension during ejection with respect to the LVEDD. Septal and posterior wall thickness were measured at end-diastole and end-systole using leading edge methodology, and the thickening fraction was calculated as the segmental percentage of thickening in systole with respect to end-diastolic thickness. Left and RV long-axis amplitude was taken from the innermost to outermost points in systole and diastole, respectively. LV isovolumic relaxation time was measured as the time interval from A2 to the onset of mitral cusp separation on the mitral echogram.16 RV isovolumic relaxation time was measured as the time interval between P2 (the pulmonary component of the second heart sound) and the onset of tricuspid Doppler forward flow.

From the transmitral and transtricuspid pulsed-Doppler traces, peak early diastolic filling velocity (E wave) and late diastolic filling velocity (A wave) were measured, and the ratio of the two (E/A) was calculated. Total LV and RV filling times were measured as the total duration of transmitral and transtricuspid flow, respectively, and the ratio of each to total diastolic time was calculated. Mitral and tricuspid E-wave deceleration time was measured from the peak of the E wave to the point at which the deceleration limb crosses the baseline. From the pulmonary forward flow trace, we measured the pulmonary acceleration time as the time interval between the onset of flow and the peak flow velocity. Pulmonary total ejection time then was measured from the same traces, and stroke distance was derived. All Doppler time intervals were corrected for heart rate (HR). LV systolic and diastolic volumes were calculated using the Teicholz formula, as follows:

where EDV is end-diastolic volume and ESV is end-systolic volume. Then stroke volume (SV) = EDV - ESV, and cardiac output = SV x HR.

Respiratory Physiology
FEV1 and FVC were measured with a dry spirometer (Vitalograph-S; Vitalograph; Buckingham, UK). The best value of three maneuvers was expressed as a percentage of the predicted value. FEV1 and FVC together with blood gas levels were recorded within a week of the echocardiographic examination. The policy was to have blood samples taken on room air while the patients were not receiving oxygen. However, 27 critically ill patients were receiving oxygen at the time of blood gas sampling. The results from these patients have been excluded from the data analysis involving blood gases.

Statistical Analysis
Values are expressed as mean ± SD. Patient values were compared with those of control subjects using the unpaired Student’s t test. The incidence of long-axis individual abnormalities (ie, values outside the corresponding 95% confidence limit of normal) was assessed using Fisher’s Exact Test. Linear regression analysis was used to determine the relationships among variables of cardiac function, blood oxygen level, and carbon dioxide status. For all tests, a p value < 0.05 was considered statistically significant. When multiple t tests or correlations were performed, a Bonferroni adjustment was used. Statistical analysis was performed using a standard statistical program package (StatView, version 4.5; SAS Institute; Cary, NC).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
All patients were in sinus rhythm with a tachycardia of 112 ± 18 beats/min vs 76 ± 16 beats/min in control subjects (p < 0.0001). LV dimensions, systolic function (assessed by fractional shortening and posterior wall thickening fraction), and wall thickness were all normal, although the LV fractional shortening was lower and posterior wall thickening fraction was higher in patients with CF (Table 1 ). Estimated SV was lower by 19% in patients than in control subjects (p = 0.01), but overall cardiac output was higher by a similar value (p = 0.03). LV diastolic function, represented by the relative isovolumic relaxation time to cardiac cycle length, E/A ratio, absolute velocities, and deceleration time of LV E wave were all normal (Table 2 ).


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  		Table 1. LV Dimensions and Systolic Function*

 

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  		Table 2. LV Diastolic Function*

 
The amplitude of long-axis excursion in patients was normal at the LV free wall site and septal site, but that of the RV free wall was significantly reduced (Table 3 , Fig 1 ), with values below the 95% confidence limits of normal in 75% of patients. The values of long-axis movement of the septal site were strongly related to those of the RV free wall site (r = 0.56; p < 0.01), indicating a functional interrelationship of the interventricular septum with RV function.


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  		Table 3. Long-axis Excursion*

 


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  		Figure 1. Long-axis recording at the RV free wall. Records were taken from a healthy subject (left) and a patient with CF (right). Note the depressed long-axis amplitude of excursion in the patient (right; 1.4 cm) to the healthy subject (left; 2.6 cm).

 
RV diastolic function, represented by the ratio of isovolumic relaxation time to cardiac cycle length, was longer in patients than in control subjects (Table 4 ). Tricuspid E-wave deceleration time was also longer in patients, but this difference did not achieve statistical significance. Pulmonary flow acceleration time and systolic stroke distance in patients with CF were both lower than normal (Table 4) . Six of the 103 patients had delayed onset of tricuspid flow with respect to P2, suggesting increased pulmonary arterial pressure (> 85 ms [ie, the upper limit of the 99% confidence interval of healthy subjects).17 In another 16 of the 103 patients, tricuspid regurgitation was detected with a peak pressure drop across the valve of > 35 mm Hg, also suggesting pulmonary hypertension.


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  		Table 4. RV Inflow and Outflow Values*

 
The FEV1 was recorded within the same week as the echocardiogram in 92 patients, and the FVC was recorded in 78 patients. Their mean FEV1 percent predicted was 20.3 ± 5.3%, and the mean FVC percent predicted was 36.2 ± 10.7%. The measurement of arterial blood gas levels was performed on air within the same week as the echocardiogram in 71 patients. The mean PaO2 was 7.20 ± 1.32 kPa (54.0 ± 9.9 mm Hg; range, 4.20 to 11.45 kPa [31.5 to 85.9 mm Hg]), and the mean PaCO2 was 6.30 ± 1.04 kPa (47.3 ± 7.8 mm Hg; range, 3.70 to 10.10 kPa [27.8 to 75.8 mm Hg]). Linear regression analysis revealed a close relationship between the amplitude of long-axis excursion at the RV free wall and the level of PaO2 (r = 0.63; p < 0.02) and PaCO2 (r = -0.68; p < 0.01).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Previous Studies
Previous echocardiographic studies in CF patients have concentrated mainly on structural abnormalities using the M-mode technique, demonstrating increased RV wall thickness and dimensions and abnormal systolic time intervals.11 18 19 A scoring system combining these echocardiographic abnormalities was found to correlate well with the clinical severity of the disease.20

In a more recent evaluation using two-dimensional and Doppler echocardiography,12 RV and LV systolic function were found to be preserved in patients with moderately severe CF. Chipps et al,13 using radionuclide angiography, demonstrated an abnormal RV ejection fraction in 13 of 18 patients with CF. Matthay et al,10 however, used the same technique and found an abnormal RV ejection fraction only in patients with severe disease (Shwachman-Kulczycky clinical score, 42 ± 4). This observation was confirmed by other investigators21 who showed marked RV dilation and flattening or compression of the ventricular septum in the majority of patients with advanced lung disease and clinical evidence of right-sided heart failure.

However, Fraser et al9 found no significant RV dysfunction in 18 CF patients with severe lung disease, although 7 of these patients had evidence of increased pulmonary artery systolic pressure. Vizza et al22 estimated the cardiac abnormalities in patients with severe pulmonary disease, and they found RV dysfunction in the majority of patients with CF and tricuspid regurgitation in 7 of 28 patients with this disorder. They also reported a significantly higher cardiac index in the CF group, the reason for which was unclear.22

LV dysfunction is generally regarded as rare in CF patients, even in those with severe pulmonary disease.9 11 12 22 There is, however, evidence of LV dysfunction in these patients. LV diastolic filling patterns have been found to be significantly different in patients with CF than in healthy subjects, which correlated with worsening pulmonary disease.23 De Wolf et al24 have reported regional myocardial perfusion defects during exercise in patients with severe CF, but the cause for this, and whether it is associated with regional cardiac dysfunction, is not fully understood.

Present Study
In this study, we examined the RV and LV systolic function in patients with CF using quantitative Doppler echocardiographic examination combined with phonocardiography, which enabled us to determine a variety of diastolic indexes. The study also was carried out on a relatively large number of adult patients with severe lung disease due to end-stage CF, who were awaiting lung or heart and lung transplantation.

Our results confirm the presence of significant RV systolic and diastolic dysfunction in the setting of consistent tachycardia and increased cardiac output. The study, however, failed to detect any specific LV abnormalities in these patients. A strong relationship between the RV systolic dysfunction, expressed by the amplitude of long-axis excursion at the RV free wall, and the degree of hypoxemia and hypercapnia, expressed by PaO2 and PaCO2, also was found.

Mechanisms
A number of possible mechanisms might be considered to explain these findings. Pulmonary hypertension has a major effect on RV function and has been shown to be associated with increased mortality in patients with CF.9 We were able to document the presence of pulmonary hypertension in 22 of the 103 patients studied. In addition, hypoxemia is an important factor that is known to affect RV function in patients with CF.7 8 9 Both intermittent and sustained hypoxemia have been implicated in the pathogenesis of pulmonary hypertension in animal models17 25 and in humans with obstructive sleep apnea and COPD.26 Furthermore, the correction of hypoxemia with supplemental oxygen therapy has been shown to reverse the progression of pulmonary hypertension in patients with COPD.27 The consistent tachycardia and increased cardiac output could be an intermediate stage in the pathway between hypoxemia and RV dysfunction and could be aggravated by recurrent infection, which is commonly seen in these patients. The strong relationship between the degree of hypoxemia and hypercapnia and the RV systolic dysfunction, as seen in this study, suggests that alterations in RV function were not simply random or due to measurement error but, more likely, were a consequence of the combination of long-standing hypoxia and increased pulmonary vascular resistance.

Study Limitations
This study was based on retrospective data, although all measurements of RV and LV function were made by the same doctor, using identical equipment and techniques. LV dimensions were obtained from the subcostal view in only 15 of 103 patients, possibly introducing extra measurement error. This effect was minimized by limiting the range of measurements in these patients to the reliably precise ones. Before undergoing echocardiography, some of the patients were taking ß-agonists, which might cause tachycardia and increased cardiac output, but it is unlikely to have affected the other echocardiographic parameters. Furthermore, all Doppler time intervals were corrected for HR. Cardiac output was derived from the LV EDV and ESV, which were calculated using the standard dimension cubed formulas that assume that the ventricle is an ellipsoid. This method could overestimate the size and volumes of the ventricle and, hence, the resulting estimated cardiac output. Again, in the absence of cavity deformity due to any other pathologic condition, these measurements should be satisfactory in representing LV function.

Since these patients subsequently underwent heart and lung transplantation, lung transplantation, or died, no long-term follow-up was possible. However, this study of a large number of patients with severe CF confirms the presence of significant RV dysfunction but no evidence of LV disease.

Unfortunately, the exact number of patients receiving long-term home oxygen therapy was not known. This may be a possible confounding factor when analyzing the echocardiographic data.


   Footnotes
 
Abbreviations: CF = cystic fibrosis; E/A = ratio of early diastolic filling velocity to late diastolic filling velocity; EDV = end-diastolic volume; ESV = end-systolic volume; HR = heart rate; LV = left ventricular; LVEDD = left ventricular end-diastolic dimension; LVESD = left ventricular end-systolic dimension; RV = right ventricular; SV = stroke volume

This research was supported by a research fellowship from the European Society of Cardiology (Dr. V. Florea), by a training fellowship from the European Society of Cardiology (Dr. N. Florea), by the British Heart Foundation (Mr. Sharma), and by the Viscount Royston Trust (Dr. Coates).

Received for publication September 28, 1999. Accepted for publication May 23, 2000.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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