ISSN : 1301-5680
e-ISSN : 2149-8156
Turkish Journal of Thoracic and Cardiovascular Surgery     
Effectiveness of echocardiographic evaluation of lung transplant candidates: Could it be an alternative to right heart catheterization?
Pınar Atagün Güney1, Murat Ersin Çardak1
1Lung Transplantation, Kartal Koşuyolu High Speciality Educational and Research Hospital, Istanbul, Türkiye
DOI : 10.5606/tgkdc.dergisi.2022.21855

Abstract

Background: In this study, we aimed to evaluate the value of transthoracic echocardiography in the estimation of pulmonary artery pressure and to identify the presence of pulmonary hypertension in lung transplant candidates with end-stage lung disease.

Methods: Between January 2012 and September 2020, a total of 244 patients (166 males, 78 females; mean age: 48.6±13.8 years; range, 18 to 77 years) who were diagnosed with end-stage lung disease due to various underlying conditions and underwent right heart catheterization and transthoracic echocardiography within 72 h were retrospectively analyzed. Hemodynamic parameters of the patients were compared. Correlation analysis was performed among the values estimated by transthoracic echocardiography and measured by right heart catheterization for pulmonary artery pressure measurements.

Results: The median pulmonary artery systolic pressure with right heart catheterization was 43 mmHg and 40 mmHg using transthoracic echocardiography. A positive correlation was seen between the pulmonary artery systolic pressure estimated by transthoracic echocardiography and right heart catheterization (r=0.718; p<0.001). The sensitivity, specificity, and positive and negative predictive values of pulmonary artery systolic pressure measurement were 76.30%, 64.22%, 72.54%, and 68.63%, respectively.

Conclusion: This study revealed a strong positive correlation between the pulmonary artery systolic pressure evaluated with transthoracic echocardiography and measured with right heart catheterization. Pulmonary hypertension detection by these two methods showed acceptable sensitivity and specificity. Transthoracic echocardiography may be a useful and practical method to monitor pulmonary artery pressure trends both initially and in the subsequent follow-up of cardiac hemodynamics in lung transplant candidates.

Pulmonary hypertension (PHT) refers to high blood pressure in the lungs, and five groups of PHT have been identified based on different etiologies. Pulmonary hypertension impairs health-related quality of life (QoL), often signals advanced pulmonary disease, and can result in early mortality if left untreated during the course of pulmonary vascular disease, lung parenchyma, or airway disease.[1] D tection of PHT is typically an indicator of a poor prognosis. Since a variety of etiologies can lead to the development of PHT, classifying patients and assessing the clinical outcomes is complex. The prognosis is associated with the underlying disease, with the worst prognosis seen in cases of PHT due to lung diseases, such as chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis (IPF).[2]

Some medical treatment is available for PHT; however, surgery is often necessary. The severity of PHT affects decisions regarding surgical options to treat end-stage lung disease. The presence of significant PHT often requires evaluation of suitability for lung transplantation (LTx).[2] The most appropriate time for LTx is determined based on the PHT diagnosis and an increasing trend in pulmonary artery pressure (PAP) values.[3]

Right heart catheterization (RHC) and transthoracic echocardiography (TTE) are routine tests performed in patients undergoing transplant assessment at LTx centers. Although RHC is the goldstandard method to measure pulmonary pressure, it is invasive, expensive, and requires an experienced team and equipment. It also has significant risks, including morbidity (1.1%) and mortality (0.055%).[4] Transthoracic echocardiography is an inexpensive, non-invasive, and practical method to estimate PAP and monitor cardiac functions. It has become a popular means of non-invasive pulmonary artery systolic pressure (PASP) evaluation in the last two decades and provides useful information about right ventricular structure and function.[5] Additionally, a study by Buyukbayrak et al.[6] showed that the TTE played a critical role in the assessment of postoperative hemodynamic impairment in open-heart surgical patients. Another important aspect of TTE is that it can facilitate prediction of hemodynamic changes that may occur following transplantation and is helpful in the postoperative patient management.[7-10] Current guidelines recommend TTE for the evaluation of LTx candidates.[11]

Lung transplantation has evolved into a life-saving treatment option that can increase survival and QoL in selected patients with end-stage lung disease.[10] An accurate PASP estimation using TTE without the need for an invasive procedure such as RHC would be of great benefit. In the present study, we aimed to analyze the correlation between PAP estimated by TTE and RHC to evaluate the performance of TTE in the estimation of PAP and to identify the presence of PHT in LTx candidates with end-stage lung disease.

Methods

This single-center, retrospective cohort study was conducted at the Department of Lung Transplantation of Kartal Koşuyolu High Speciality Educational and Research Hospital between January 2012 and September 2020. The study included a total of 244 consecutive patients (166 males, 78 females; mean age: 48.6±13.8 years; range, 18 to 77 years) who were diagnosed with end-stage lung disease due to various underlying conditions such as obstructive lung disease (OLD), interstitial lung disease (ILD), end-stage infectious lung disease, or pulmonary vascular disease (PVD), who were referred for LTx. Of the initial 317 patients selected for the study, 11 were excluded, as TTE and RHC were not both performed within 72 h. Another 38 patients were eliminated, as PASP could not be estimated using TTE, and 24 patients were found not to have sufficiently appreciable tricuspid regurgitation. Finally, 73 patients were excluded due to insufficient data for this study. The study flow chart is shown in Figure 1.

Figure 1. Study flow chart.
TTE: Transthoracic echocardiography; RHC: Right heart catheterization; PASP: Pulmonary artery systolic pressure; LVEF: Left ventricular ejection fraction; PAP: Pulmonary artery pressure; CO: Cardiac output; CI: Cardiac index; NIMV: Non-invasive mechanical ventilation; 6MWD: 6-min walking distance; BSA: Body surface area.

Data collection The data used were extracted from patient files and the hospital database. Patient demographic details, smoking history, body mass index (BMI), arterial blood gas values, results of respiratory function test and a 6-min walk test (6MWT), long-term oxygen therapy use, need for non-invasive mechanical ventilation, PASP estimated by TTE, PASP measured by catheter, PAPmean, cardiac output (CO) results, and cardiac index (CI) assessments were recorded.

Standard procedures
The 6MWT was performed without any oxygen assistance according to the American Thoracic Society (ATS) guideline by an experienced physiotherapist.[12]

The RHC was regulated with a balloon-tipped and flow-directed pulmonary artery catheter. The catheter was placed through the right femoral vein or the right internal jugular vein utilizing local anesthesia and the Seldinger technique. Pulmonary artery occlusion pressure, right atrial pressure, pulmonary artery systolic and diastolic pressure, and CO were each measured twice. The TTE was performed using conventional clinical echocardiographic equipment (il53 xMATRIX ultrasound system; Philips Healthcare, Inc., Andover, MA, USA). Transthoracic Doppler and two-dimensional images were retrieved from parasternal long and shortaxis, apical four-chamber, and subcostal four-chamber views. Right ventricular size and function were assessed. The color flow Doppler technique was used to discern tricuspid regurgitate flow, and maximum jet velocity was calculated with continuous-wave Doppler without intravenous contrast. The right ventricular systolic pressure was approximated according to the modified Bernoulli equation and was considered equal to PASP without right ventricular outflow obstruction: PASP (mmHg) = r ight ventricular systolic pressure = trans tricuspid gradient + right atrial pressure, where tricuspid gradient 4xv2 (v= peak speed of tricuspid regurgitation m/second).[4,13,14]

The 2015 European Society of Cardiology (ESC)/ European Respiratory Society (ERS) Guidelines for the Diagnosis and Treatment of Pulmonary Hypertension definition of PHT of a PAPmean at rest of ?25 mm Hg was used.[15]

Statistical analysis
Statistical analysis was performed using the IBM SPSS version 23.0 software (IBM Corp., Armonk, NY, USA). Descriptive data were presented in mean ± standard deviation (SD), median and interquartile range (IQR) or number and frequency, where applicable. The relationship between RHC and hemodynamic changes detected with the TTE was evaluated according to the Pearson correlation analysis. The Bland-Altman analysis was used to determine the clinical compatibility of the TTE estimates of PASP/PAPmean with the values determined by RHC, and TTE estimates of PASP/PAPmean were considered accurate at 95% limits of agreement within 10 mmHg. A p value of <0.05 was considered statistically significant.

Results

The patients were divided into subgroups according to underlying lung disease: OLD (n=64, 26.2%), ILD (n=111, 45.5%), end-stage infectious lung disease (n=55, 22.5%), and PVD (n=14, 5.7%). The mean time from diagnosis to the evaluation of the patient for a LTx candidate in the inpatient setting was 7.61±6.93 years. The mean BMI was 23.3±4.3 kg/m2 and the mean forced expiratory volume in 1 sec (FEV1) was 34.75±18%. Demographic data, pulmonary function test results, and hemodynamic characteristics of the participants are presented in Table 1 according to the underlying lung disease group. The mean age was higher in ILD and OLD subgroups than end-stage infectious lung disease and PVD groups (p<0.001). When the ILD and OLD groups (p=0.17) and end-stage infectious lung disease and PVD groups (p=0.52) were evaluated among themselves, there was no statistically significant difference. However, smoking was significantly higher in the ILD group than in the OLD, end-stage infectious lung disease, and PVD groups (p<0.001). End-stage infectious lung disease according to the time elapsed after diagnosis; ILD was short compared to OLD and PVD (p<0.001). The mean FEV1 in ILD group was higher than that of the OLD and end-stage infectious lung disease subgroups (p<0.001), but no significant difference was found compared to the PVD subgroup (p=1.00). The mean FEV1 value was similar in the OLD and end-stage infectious lung disease (p=1.00) groups and in the PVD and other disease groups (p=0.93). There was no statistically significant difference among the subgroups in terms of the mean BMI and 6MWT values (p=1.00 and p=1.00, respectively). The mean TTE PASP value was higher in the PVD group than that of the ILD, OLD, and end-stage infectious lung disease groups (p<0.001). The mean PASP value measured with the RHC was higher in the PVD group than that of the ILD, OLD, and end-stage infectious lung disease groups (p<0.001). The mean CO and CI values were similar among the subgroups (p=1.00 and p=1.00, respectively).

Table 1. Demographic and clinical data of patients

The median RHC PASP value was 43 (IQR: 33 to 56.75) mmHg, while it was 40 mmHg (IQR: 30 to 60) mmHg when TTE was used. The TTE results indicated a median left ventricular ejection fraction of 63.56% (IQR: 63.09 to 64.03%), a median CO of 4.5 L/min (IQR: 4.3 to 4.6 L/min), and a median CI of 2.5 L/min/body surface area (BSA) (IQR: 2.5-2.6 L/min/BSA). The RHC and TTE hemodynamic measurements are presented in Table 2.

Table 2. Hemodynamic parameters determined by RHC and Doppler echocardiography

Overall, 55.3% (n=135) of the study patients were diagnosed with PHT based on RHC measurements, while 58.2% (n=142) were diagnosed with TTE. Figure 2 shows the PASP values recorded by TTE and RHC for each of the subgroup. The overall median PASP was 40.0 (IQR: 45.57 to 52.33) mmHg as assessed by TTE and 43 (IQR: 33 to 56.75) mmHg as measured by RHC. The patients with ILD had a median PASP of 44 (IQR: 30 to 60) mmHg using TTE and the median RHC measurement was 43.0 (IQR: 31 to 53) mmHg. Patients with OLD had a median TTE PASP of 35 (IQR: 29 to 45) mmHg and the median RHC PASP was 38 (IQR: 33 to 51) mmHg. The end-stage infectious lung disease patients had a median PASP of 43 (IQR: 29 to 65) mmHg using TTE and a median of 46.0 (IQR: 35 to 58) mmHg using RHC. The PVD group had a median PASP by RHC of 93 (IQR: 76 to 138) mmHg.

Figure 2. PASP in the sub-groups according to etiology of lung disease. First two groups estimated by TTE, last two groups measured by RHC.
PASP: Pulmonary artery systolic pressure; TTE: Transthoracic echocardiography; RHC: Right heart catheterization; PASP: Pulmonary artery systolic pressure.

Correlation analysis of TTE and RHC PASP measurements are shown in Table 3. A strong correlation between the two methods was seen in all of the study patients (r=0.718; p<0.001) (Figure 3). The Bland-Altman analysis results are illustrated in Figure 4. Analysis according to the underlying lung disease subgroups revealed a weak correlation in OLD patients (r=0.416; p=0.001) and a moderate correlation in the ILD (r=0.647; p<0.001) and end-stage infectious lung disease (r=0.590; p<0.001) groups. No significant correlation was observed in the PVD patients (r=0.428; p=0.127).

Table 3. Correlation between RHC and TTE PAP values in subgroups*

Figure 3. Correlation between pulmonary artery systolic pressure estimated by TTE and measured by RHC in lung transplantation candidates.
RHC: Right heart catheterization; TTE: Transthoracic echocardiography.

Figure 4. Bland-Altman plot of pulmonary artery pressure measurements by RHC and estimations by TTE.
RHC: Right heart catheterization; TTE: Transthoracic echocardiography.

The sensitivity, specificity, and positive predictive and negative predictive values of TTE and RHC were analyzed based on the PHT criteria. The sensitivity, specificity, and positive and negative predictive values of PASP for a diagnosis of PHT using TTE was 76.30% (confidence interval [CI]: 68.22-83.19%), 64.22% (CI: 4.47-73.17%), 72.54% (CI: 66.88-77.55%), and 68.63% (CI: 61.05-75.33%), respectively (Table 4). Due to the small sample size, the PVD group was not included in the analysis.

Table 4. Sensitivity, specificity, and positive and negative predictive values of PAPs by Doppler echocardiography for diagnosis of pulmonary hypertension

Discussion

The main finding of this study is that the results of TTE PASP assessment correlated with the RHC measurements with an acceptable sensitivity (76%) and specificity (64%) in transplantation candidates with end-stage lung diseases. Therefore, TTE can be used to non-invasively evaluate pulmonary hemodynamics. However, the results also demonstrated that the correlation between TTE and RHC measurements of PAP differed in specificity and sensitivity according to the underlying lung disease. Although RHC is the gold standard for PHT, it is an invasive method that requires extensive equipment and limited application.[15] The TTE provides information about functional cardiac changes that may affect perioperative management in transplant candidates, as well as estimation of PAP. In addition, it can be used for PAP monitoring due to its reproducibility. The use of echocardiography in clinical practice may provide great value for transplant patients.

Previous studies have examined the correlation between TTE and RHC measurement of PASP in non-transplantation patients with various underlying diseases. Kim et al.[16] reported a strong correlation between PAP measured with TTE and RHC in patients with end-stage liver disease (r=0.718; p<0.001; sensitivity: 97%, specificity: 77%). In a recent study by Sohrabi et al.,[17] the PAP estimated by TTE correlated with RHC values in patients with rheumatic mitral valve stenosis (r=0.89; p<0.001; sensitivity: 92.8%, specificity: 86.6%).

The widespread application of LTx in many centers has led to greater use of TTE in clinical practice in the last decade. Recent studies have examined the correlation between TTE and RHC measurements of PAP in LTx candidates. Both Arcasoy et al.[2] and Ben-Dor et al.[18] reported a strong correlation (r=0.69; p=0.0001 and r=0.80; p<0.0001, respectively). Similarly, in our study, we found that the PAP values of both methods were strongly correlated in LTx candidates (r=0.71; p<0.001). Arcasoy et al.[2] reported a PHT prevalence of 25% using RHC and 44% using TTE, with a mean PASP of 49.08±24.13 mmHg using RHC and a mean of 48.95±26.78 mmHg using TTE. In contrast, we found that 93.9% of all patients were diagnosed with PHT with RHC and 58.2% with TTE. This difference can be explained by the fact that the PAP threshold value for the diagnosis of PHT, which is higher than that used in our study, is ?45 mmHg. Similarly, the median PASP using TTE was 40.0 mmHg and 43 mmHg using RHC in our study. In the Arcasoy et al.'s[2] study, the estimation of PASP by TTE had an 85% sensitivity, 55% specificity, and 52% positive and 87% negative predictive values, which are similar to our rates (76.3%, 64.22%, 72.54%, and 68.63%, respectively).

In the present study, PAP values could not be obtained by TTE for 62 patients due to a poor tricuspid regurgitation signal or other technical inadequacies. The PAP estimation by TTE was possible in 76.9% of our patients. Ben-Dor et al.[18] reported TTE PASP evaluation of 74% in their study. Arcasoy et al.,[2] however, used TTE in only 44% patients, which we speculate that it may be a result of differing equipment quality and experience level in multiple specialists.

Difficulties associated with TTE assessment of pulmonary hemodynamics include obtaining insufficient echocardiographic images in a hyperinflated chest and potential rightward rotation of the heart, and difficult visualization of the tricuspid valve and vena cava in patients with obstructive lung disease due to the physiology of the disease. Fisher et al.[19] evaluated patients with severe emphysema and found that TTE and RHC PAP values were weakly correlated and the test characteristics (sensitivity, specificity, and predictive values) were poor for TTE diagnosis of PHT. They reported that the diagnosis of PHT was important in patients with emphysema and that TTE should be interpreted carefully and may need to be confirmed with RHC. The examination according to underlying disease in our transplant candidates revealed a noteworthy poor correlation between the two methods in OLD patients compared to the ILD and end-stage infectious lung disease groups (r=0.416 p=0.001; r=0.647, p<0.001; and r=0.590, p<0.001, respectively). The sensitivity and specificity of patients with OLD were also relatively low (41.67% and 75%, respectively). Our results are consistent with those of Arcasoy et al.,[2] despite the relatively low sensitivity and specificity rates due to poor image quality in the patient group with hyperinflation, and TTE may be preferable for LTx and perioperative management.

A long wait for listed LTx candidates contributes to annual mortality.[20] Pulmonary hypertension is a major risk factor for early and late mortality in LTx patients.[21] Mortality varies according to the underlying disease, and wait list mortality can be as much as 64%, particularly in cases of IPF. Nathan et al.[22] investigated transplant candidates with IPF and revealed that the incidence of PHT increased from 77 to 86% during the period between diagnosis and transplantation. Keir et al.[23] also estimated nearly 90% PHT in patients with non-transplant ILD using TTE. In our study, the correlation between TTE and RHC was higher in ILD patients compared to other underlying disease groups (r=0.647; p<0.001).

Right heart catheterization may be risky in detecting PHT in ILD patients due to the frequent accompanying cardiac hemodynamic disorders. Thus, TTE can be safely used as a non-invasive method for detecting PHT in these patients, as it enables the evaluation of cardiac parameters. According to our results, the TTE and RHC correlation of PASP measurement was higher in ILD patients compared to other underlying disease groups (r=0.647; p<0.001). Therefore, echocardiographic evaluation of cardiac hemodynamics in ILD patients who are candidates for transplant has a critical value.

To avoid the development of PHT, it is of utmost importance to refer this patient group for transplantation soon after diagnosis and to reduce the time on the waiting list as much as possible. In our study, the mean time after diagnosis in patients who are still waiting for LTx and who underwent LTx was 7.6±6.9 years. Among these, the patient groups with the shortest waiting time were PVD (3; 95% CI: 1-7) and IPF (5.1±3.8 months).

One of the main limitations to this study is that there is a 72-h time frame allowed for the use of the two methods. The PAP is a dynamic measurement and can vary up to 30% within 24 h as reported by Rich et al.[24] Another limitation is that, although we could not monitor and provide oxygen as needed during the RHC procedure, we were unable to monitor oxygen saturation or provide standardized oxygen during TTE. Hypoxemia that occurs during testing can cause pulmonary vasoconstriction.

In conclusion, our study results showed that pulmonary artery systolic pressure assessed using transthoracic echocardiography was strongly correlated with that measured using right heart catheterization in transplant candidates. These results suggest that transthoracic echocardiography may be a very useful, practical, non-invasive method of monitoring pulmonary artery systolic pressure changes, particularly in idiopathic lung disease patients, in the assessment of pulmonary hypertension and cardiac hemodynamics. In the obstructive lung disease group, due to transthoracic echocardiography imaging difficulties, evaluation of transthoracic echocardiography pulmonary artery systolic pressure may need to be confirmed by right heart catheterization.

Ethics Committee Approval: The study protocol was approved by the Kartal Koşuyolu High Speciality Educational and Research Hospital Ethics Committee (date: 06.10.2020, no: 2020/9/365). The study was conducted in accordance with the principles of the Declaration of Helsinki.

Patient Consent for Publication: A written informed consent was obtained from each patient. Data Sharing Statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions: Idea/concept, literature review: M.E.Ç.; Design, data collection and/or processing, analysis and/or interpretation, writing the article: P.A.G.; Control/ supervision, critical review, references and fundings, materials: P.A.G., M.E.Ç.

Conflict of Interest: The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding: The authors received no financial support for the research and/or authorship of this article.

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Keywords : Lung transplantation, right heart catheterization, transthoracic echocardiography
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