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Eur J Cardiothorac Surg 2004;26:508-514
© 2004 Elsevier Science NL

Study on the late effect of pneumonectomy on right heart pressures using Doppler echocardiography

^a Second Department of Thoracic Surgery, Athens Chest Diseases Hospital ‘Sotiria’, 152 Messogion Avenue, 11527 Athens, Greece
^b Department of Cardiology, Athens Chest Diseases Hospital ‘Sotiria’, 152 Messogion Avenue, 11527 Athens, Greece

Received 22 February 2004; received in revised form 15 May 2004; accepted 24 May 2004.

^* Corresponding author. Address: Athens Chest Diseases Hospital, 35 Ioustinianou Street, 41223 Larissa, Greece. Tel.: +30-241-287-466/944-910-343; fax: +30-241-611-097
e-mail: foroulis{at}internet.gr

	Abstract

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
Objective: Changes in the pulmonary artery systolic pressure (PASP) and the dimensions of the right ventricle (RV) of the heart, six months after pneumonectomy, were evaluated in order to detect the influence of pneumonectomy on right heart function. Methods: 35 patients undergoing pneumonectomy (Group A) and 17 patients undergoing lobectomy or bilobectomy (Group B) were evaluated prospectively with spirometry, arterial blood gases determination and Doppler echocardiography at rest, preoperatively and six months postoperatively. Patients of both groups had normal preoperative PASP, RV dimensions and left ventricular ejection fraction. PASP was calculated using the equation: PASP=4x(maximal velocity of the tricuspid regurgitant jet)²+10 mmHg. FEV₁, FVC, partial pressures of oxygen (pO₂) and carbon dioxide in the arterial blood were considered as the main determinants of postoperative lung function. Results: PASP increased significantly six months postoperatively in both groups (P<0.05). Mean PASP in Group A (40.51±12.52 mmHg) was significantly higher (P=0.012) than in Group B (32.88±5.25 mmHg). Mean PASP after right pneumonectomy (48.33±10.61 mmHg) was significantly higher (P=0.002) than after left pneumonectomy (35.26±10.83 mmHg). The incidence of RV dilatation was higher in Group A (60%) than in Group B (23.52%). RV dilatation was related with elevated PASP values in both groups (P<0.001 and P=0.034, respectively). Increased age (P<0.001), significant percent FVC reduction from preoperative values (P=0.012) and low pO₂ values (P=0.001) were detected as strong predisposing factors for postpneumonectomy PASP elevation. Conclusions: Pneumonectomy is related with postoperative elevation of PASP and RV dilatation, especially right pneumonectomy. Significant percent FVC reduction, increased age and low pO₂ values are the main responsible factors for elevation of the 6-month postoperative PASP values.

Key Words: Pneumonectomy • Late effects of pneumonectomy • Right ventricular systolic pressure • Pulmonary artery systolic pressure • Doppler echocardiography • Tricuspid regurgitation

	1. Introduction

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
In the past, the late effects of major lung resection on right heart function have not been well established [1–3]. Pneumonectomy results in considerable decrease of the pulmonary vascular bed, with subsequent increase of the perfusion to the remaining lung and of the right ventricle (RV) afterload. Research studies in dogs as well in humans on the late effects of pneumonectomy on the right heart function and on the mean Pulmonary Artery Pressure (mPAP) at rest, using right heart catheterization, detected moderate increase in mPAP when compared to the baseline values [1–5]. Postoperative elevation of pulmonary artery pressure has also been documented in the modern thoracic surgery for lung cancer [1]. However, in all recent publications, where changes in mPAP after pulmonary parenchyma resection have been studied in humans, deal with the time immediately after the pulmonary artery clamping or the early postoperative period [1–3,6].

Right heart catheterization has been used for the evaluation of right heart function after pneumonectomy, but it has the risk of pulmonary artery rupture, mainly when pulmonary hypertension is present [7,8]. In addition, it is not always easy to insert the catheter into the right ventricle, when severe tricuspid regurgitation (TR) is present [7,8]. Taking into consideration all of these reasons right heart catheterization should be avoided in postpneumonectomy patients, as the tool to evaluate right heart function. Continuous Wave Doppler Echocardiography (CWDE) has been successfully used during the last two decades for the estimation of right heart pressures in patients suffered from Chronic Obstructive Pulmonary Disease (COPD) [8–12]. Also, CWDE has been used for the estimation of Pulmonary Artery Systolic Pressure (PASP) during the lung parenchyma resection perioperative period and for the determination of the causes of postoperative arrhythmias, after non-cardiac thoracic surgery [6,13]. In the present study, the influence of the amount of lung parenchyma resection on right heart pressures and right heart dimensions were evaluated by using CWDE, six months after pneumonectomy and less extended than pneumonectomy pulmonary parenchyma resection. The influence of postoperative lung function on right heart pressures was also evaluated.

	2. Methods

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
2.1. Patients—study design
Forty-two well-selected patients undergoing pneumonectomy for lung cancer between 1/1996 and 6/2000, were evaluated preoperatively (within the last preoperative week) and six months postoperatively with spirometry, CWDE and arterial blood gasses determination. All the referred laboratory examinations were performed at rest of the patients. Seventeen patients who underwent less than pneumonectomy pulmonary parenchyma resection for lung cancer during the same period (lobectomy or bilobectomy), were also evaluated using the same protocol and were included in the study as controls (Group B). Pulmonary parenchyma resection was performed through a standard posterolateral thoracotomy incision and one-lung ventilation. All patients had preoperatively sinus rhythm at electrocardiogram, normal PASP, RV dimensions and left ventricular ejection fraction (LVEF) equal or more than 55% at echocardiography. No patient had preoperatively clinical or echocardiographic evidence of aortic or mitral valvular heart disease or previous open-heart surgery for correction of cardiac abnormalities, ischemic or valvular heart disease. A normal exercise electrocardiogram test within the last one-year preoperative period was necessary to include a patient into the study protocol. Recurrent mediastinal disease was excluded by performing chest CT scan six months postoperatively. Also, there was no clinical evidence of metastasis elsewhere in the body six months after the operation.

Patients who had serious postoperative complications such as bronchopleural fistula or empyema, respiratory failure or acute myocardial infarction, were excluded from the study protocol. Four patients from Group A were excluded from the study protocol during the study process, because of the development of serious postoperative complications (bronchopleural fistula in 2 cases, postoperative respiratory distress in 2 cases). Also, there were excluded two patients who ignored the follow-up procedure and one patient who got discharged from the hospital the 8th postoperative day and he died 73 days later (unknown cause of death). The final TNM staging of patients is presented in the Table 1. Patients with IIIA disease received 4–6 cycles of platinum-based adjuvant chemotherapy.

Six months postoperatively, patients of both groups were classified into four classes of dyspnea on exertion, according to a standard questionnaire:

• Class 1: No dyspnea or dyspnea only on heavy exertion
  
• Class 2: Dyspnea on moderate exertion (stair climbing more than two flights)
  
• Class 3: Dyspnea on mild exertion (stair climbing less than one flight)
  
• Class 4: Dyspnea at minimal exertion or at rest (incapacitating)
  

2.2. Echocardiography
All the patients of both groups who participated in the study underwent two-dimensional echocardiograms, which were performed by one of three experienced cardiologists (echocardiographers). All Doppler echocardiograms were performed one to seven days prior to surgery and six months after the operation. Echocardiographic studies were performed using an Aloca SSD-860 ultrasound machine (ALOCA Co Ltd, Japan) with a 2.5 Mhz imaging/continuous-wave Doppler and color Doppler transducer. Doppler recordings were attempted using the apical four-chamber view and subcostal long axis view of the heart. Initially, tricuspid regurgitation jet was localized with color flow Doppler and then interrogated with image-directed continuous-wave Doppler. A systematic search was performed to identify the best recording of the greatest maximal velocity. The systolic trans-tricuspid pressure gradient (P) was calculated using the modified Bernoulli equation: P=4V_max², where V_max represents the maximal tricuspid regurgitant velocity in m/s. V_max for each patient was calculated as the average peak velocity among five consecutive calculations. PASP was calculated as the sum of the trans-tricuspid gradient and the estimated right atrial pressure (RAP). RAP was substituted in the equation by a fixed empirical value of 10 mmHg, as suggested by Currie et al. [14]. PASP is equal to the RVSP in the absence of pulmonary outflow obstruction and subsequently PASP=RVSP=4V_max²+10 mmHg. If tricuspid regurgitation (TR) was absent or insignificant according to the CWDE examination, PASP was considered to range in normal values (25 mmHg). Trace regurgitations or TR jets limited to the proximal to the valve one fourth of the right atrium were considered as insignificant jets. Intravenously injected contrast was not used to augment the spectral Doppler signals of TR. If PASP values 30 mmHg were calculated on CWDE 6-months postoperatively, patients were considered to have influenced right heart pressures, as the result of pulmonary parenchyma resection, RV was considered to be ‘normal’ if it had dimensions less than 25 mm, ‘dilated to the upper normal limits’ if it had dimensions between 25 and 28 mm and ‘dilated in abnormal levels’ if it had dimensions more than 28 mm.

2.3. Spirometry and arterial blood gases determination
Spirometric data of patients (FEV₁ and FVC) were obtained using the Morgan Spiro 232 (PK Morgan Ltd, Gillingham, Kent, England). For the arterial blood gases determination, blood samples were taken via puncture of the radial artery and were, immediately after puncture, analyzed in the CIBA-CÖRNING 288 blood gases analyzer (CIBA-CÖRNING prognostics group, USA).

2.4. Statistical analysis
Comparison between two percentages has been done using the ² or Fisher's exact test. Comparison between the mean values of two different groups of patients has been done using the independent samples t-test and comparison among the mean values of 3 or more different groups has been done using the one-way analysis of variance test (one-way ANOVA). Changes between preoperative and postoperative PASP in the same group were analyzed using the sign test, where the following considerations were accepted, when TR was absent or insignificant and PASP could not be calculated: (a) preoperative absence of TR and postoperative measured PASP 25 mmHg or postoperative absence of TR was accepted as a tie, (b) preoperative TR absent and postoperative measured PASP 30 mmHg was accepted as a positive difference. The strength of the influence of the considered predictor parameters on postoperative PASP has been estimated using the ordinary regression analysis, and the results were verified through its non-parametric analogue (regression on the ranks). P-values less than 0.05 were considered as significant values.

	3. Results

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
The two groups of patients were similar regarding their age, preoperative percent of the predicted first second force expired volume (FEV₁), percent of the predicted forced expiration using maximum effort (FVC) and partial pressures of oxygen (pO₂) and carbon dioxide (pCO₂) in the arterial blood (Table 2).

PASP was found to strongly deviate from normal levels (35 mmHg) in all patients six months after right pneumonectomy and in 35.79% of patients six months after left pneumonectomy. In 26.08% of patients six months after left pneumonectomy PASP was found to deviate easily from normal levels (30 mmHg) and it was found to range in normal levels (25 mmHg) in the rest 38.13%.

When TR was postoperatively Doppler-detected, the mean calculated PASP in the pneumonectomy Group (Group A) had significant difference with the mean calculated PASP in the lobectomy/bilobectomy Group (Group B). The mean measured PASP after right pneumonectomy had significant difference when compared to the mean measured PASP after left pneumonectomy. No differences were found between the mean measured PASP after standard and intrapericardial pneumonectomy and after left pneumonectomy and lobectomy/bilobectomy. These results are presented in the Table 5. The six months postpneumonectomy PASP was positively influenced by the percent change (negative values) from baseline of FVC (parameter estimate=–26.45, P=0.012) and age (parameter estimate=0.8158, P=0.0004), while it was negatively influenced by postoperative pO₂ values (parameter estimate=–0.388, P=0.0012).

3.4. Class of dyspnea on exertion and PASP
In Group A, the mean PASP of patients with Class 4 dyspnea on exertion (65.00+7.07 mmHg) had significant difference with the mean PASP of patients with Class 1 (35.40+8.55 mmHg), Class 2 (39.80+10.40 mmHg) and Class 3 (41.55+13.91 mmHg) dyspnea on exertion (one-way ANOVA: F=4.111,P=0.016/LSD multiple comparison test).

In Group B, all patients with Class 1 dyspnea on exertion had not TR and PASP was considered to be normal. Only one patient from Group B had Class 4 dyspnea on exertion and his 6 months postoperative PASP was found to be 70.00 mmHg. The mean PASP of patients with Class 3 (35.20+5.26 mmHg) and Class 2 (28.50+4.87 mmHg) dyspnea on exertion had not significant difference (T-test: t=–1.617,P=0.150).

	4. Discussion

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 
Echocardiography is a reliable, non-invasive technique for the estimation of right heart function [6,9–11]. CWDE has been used for the estimation of right heart pressures in patients with COPD, when TR was Doppler detected [8–12]. These studies demonstrated that TR velocity represented the single Doppler variable, which had good correlation with the mean PAP. Although technically easier, the less direct methods for the estimation of PASP from the acceleration time in the right ventricular outflow tract and the right ventricular isovolumic relaxation time, are less accurate than the TR jet method [9]. Doppler echocardiography is an accurate method for the estimation of right heart pressures, as it well shown in previous published studies in COPD patients, where similar results were obtained with right heart catheterization and echocardiography [9,10]. Echocardiographic estimation of PASP in patients with COPD is referred to be more accurate when it is elevated in abnormal values (more than 35 mmHg). In these studies, significant TR was found to be always present, when PASP was 35 mmHg [9,10,15]. In a previous study by Lewis et al. (1994) on changes in right heart pressures after pneumonectomy using right heart catheterization, it was well demonstrated that mPAP elevation paralleled their systolic counterpart [16]. Their regard supports the use of echocardiography for the estimation of right heart pressures after pneumonectomy.

In the era of thoracic surgery for lung cancer, Amar and co-workers (1996), by using Doppler echocardiography, found in their series a small increase in PASP after pulmonary resection, especially after pneumonectomy. Patients who underwent pneumonectomy had significantly higher PASP than that the patients who underwent lobectomy. Important RV enlargement was observed in this study only in patients with postoperative respiratory distress. However, they performed early postpneumonectomy calculation of PASP in their patients (between the 2nd and the 6th postoperative day). They also highlighted the need to investigate changes in PASP after pulmonary resection within a longer horizon, than the first postoperative days. Adequate Doppler recordings were obtained in this study in 79% of postlobectomy patients and in 77% of postpneumonectomy patients on postoperative days 2 through 6 [6]. The present work adds to the study of Amar and co-workers, investigating the influence of pneumonectomy on PASP and RV dimensions six months postoperatively. Our results support the serious influence of major lung parenchyma resection on right heart function. According to the results of the present study, the extent of lung parenchyma resection plays an important role in the degree of elevation of right heart pressures. PASP had higher values after right pneumonectomy as opposed to left pneumonectomy. Also, PASP had higher values after pneumonectomy as opposed to lobectomy or bilobectomy. In a previous published series, the authors supported that the extent of lung parenchyma resection did not influenced PASP; they found that ischemic heart disease was responsible for the observed pulmonary hypertension in a serious percentage of their patients [2]. Our results do not agree with the results of the previous mentioned study, as ischemic heart disease was not a point in our patients (they all had a negative exercise electrocardiogram test within the last one year preoperative period and normal LVEF preoperatively). We strictly selected the included in the present study patients, in order to exclude factors other than the amount of pulmonary parenchyma resection (mediastinal recurrence of the tumor by performing chest CT scan at 6th postoperative month, congenital or acquired heart disease by performing preoperative electrocardiogram stress test and echocardiography), which could influence right heart pressures. Excluding other factors, except COPD, associated with elevation of right heart pressures, the observed differences in postoperative PASP between groups (pneumonectomy versus lobectomy/bilobectomy) and subgroups (right pneumonectomy versus left pneumonectomy) depends only on the different amount of pulmonary vascular bed resected in each type of operation. Intrapericardial pneumonectomies are frequently performed on the left side, and their cumulative influence on PASP is probably close to that of the left pneumonectomy.

The localization of TR jet with color flow map in all patients on behalf of the estimation of PASP had as target to exclude measurement of PASP when insignificant TR was present and to exclude the ‘door effect’ phenomenon, avoiding with this manner the trap of the ‘iatrogenic heart disease’ [17–22]. The Doppler technique is so sensitive that clinically insignificant regurgitation can be detected. The severity of regurgitation in these cases is minimal and it represents ‘nature's imperfection’ in the design of normal valve structure or myxomatous degeneration of valves and their supporting structures with increased aging [19,22]. Indeed, the separation of individuals with abnormal valvular regurgitation is possible and is based on the significant larger area of regurgitation visualized on the color flow map, the elevation of right heart pressures, the dilation of the valve annulus, the presence of structural abnormality of the valve, the presence of increased afterload conditions, such as pulmonary disease and lung parenchyma resection [21]. Significant Doppler detected TR was developed six months after the operation in 88.57 and 58.82% of patients in Group A and B, respectively, as a result of the increased blood flow to the remaining lung. Passive distention of the reduced in volume pulmonary vessels cannot balance the increased blood flow to the remaining lung, even at rest, resulting in pulmonary hypertension. The preoperative compliance of the pulmonary vascular bed plays an important role in the degree of PAP elevation [5].

In the present study, increased age, low pO₂ values and significant percent reduction of FVC from preoperative values were found to have substantial influence on postpneumonectomy PASP. Amar and coworkers found good correlation between preoperative PASP and preoperative percent of the predicted FEV₁ in their series [6]. It is well known that low pO₂ values in the arterial blood play an important role in the development of pulmonary hypertension, as low pO₂ values are a potent vasoconstrictive factor on pulmonary circulation [23]. However, none of the included in the study patients had severe hypoxemia (<60 mmHg) six months postoperatively in both groups.

In conclusion, Doppler echocardiography is a useful, non-invasive method for the estimation of right heart pressures after pulmonary parenchyma resection, which can detect patients with postoperatively affected right heart function. The majority of patients experience an elevation of PASP to abnormal levels after pneumonectomy, especially right pneumonectomy. About half of patients after lobectomy or bilobectomy experience elevation of PASP to abnormal levels. Elevated PASP values are associated with RV dilatation. Increased age and low postoperative pO₂ values have substantial influence on postoperative PASP values. Significant percent reduction of 6-month postoperative FVC values from their preoperative values is associated with increased postoperative PASP, detecting that the amount of pulmonary vascular bed resected at thoracotomy plays an important role in PASP elevation.

	Acknowledgments

 
The authors would like to thank the statistician Yannis Bassiakos, Associate Professor of Statistics-Economic University of Athens, for his assistance in the statistical analysis of the data.

	References

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Christophoros N. Foroulis Christophoros S. Kotoulas Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Foroulis, C. N. Articles by Lioulias, A. G. Search for Related Content PubMed PubMed Citation Articles by Foroulis, C. N. Articles by Lioulias, A. G. Related Collections Lung - cancer Lung - other Cardiac - other Lung - basic science