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Eur J Cardiothorac Surg 1999;15:444-448
© 1999 Elsevier Science NL


Right ventricular morphology and function after pulmonary resection1

Janusz Kowalewski, Marian Brocki, Tadeusz Dryjanski, Krzysztof Kapron, Stanislaw Barcikowski

Military Medical Academy, Lodz, Poland

Received 21 September 1998; received in revised form 14 December 1998; accepted 12 January 1999.

Corresponding author. SK WAM, ul. Zeromskiego 113, 90–549 Lodz, Poland. Tel.: +48-42-6333-890; fax: +48-42-6333-890; e-mail: wam1klch@polbox.com


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Objective: To identify the effect of pulmonary resection on right ventricular performance and its possible contribution to mortality and morbidity. Methods: Before and 2 days after pulmonary resection for primary lung cancer in 31 patients (21 males; ages 32–69 years), echocardiographic examinations of the right ventricle were performed. Systolic, diastolic and stroke volumes as well as right ventricular ejection fraction were estimated. Right ventricular volumes were calculated using the subtracting method. Results: Right ventricular end-diastolic volume index increased significantly in patients after pneumonectomy: 80.4±7.2 ml/m2 versus preoperative evaluation: 66.1±5.2 ml/m2 (P=0.031). In patients who underwent pneumonectomy right ventricular ejection fraction significantly decreased from 48±5.0% preoperatively to 39%±4.1% after surgery (P=0.027). Fourteen patients after pneumonectomy had development of supraventricular arrhythmias postoperatively. These patients had much higher right ventricular end-diastolic volume index (76.3±6.4/82.1±7.4; P=0.032) and lower right ventricular ejection fraction (42±4.3/37±3.9; P=0.021) after surgery in comparison with patients who had normal sinus rhythm postoperatively. Conclusion: Pulmonary resection caused a significant dilatation and dysfunction of right ventricle in the early postoperative period. Early detection of deterioration in right ventricular function after pneumonectomy may provide the opportunity for interventional therapy.

Key Words: Lung cancer • Surgery • Pneumonectomy • Right ventricle • Echocardiography


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Pulmonary resection is now the best treatment for patients with lung cancer, but deterioration of cardiopulmonary function may be unavoidable after the operation [1]. The consequence of the right ventricle (RV) performance in cardiac function after pulmonary resection is emphasized in many papers [2] [3] [4] [5]. RV after such treatment is found distended and its contractility is depressed [3] [4] [6]. Supraventricular arrhythmias are well documented complications, especially common after pneumonectomy [4] [7] [8], and in selected patients they are associated with significant mortality [7]. However, the etiology of the arrhythmias has never clearly been proved [1] [7].

A simple and not invasive method for the monitoring of RV performance in the early postoperative period may be invaluable for a thoracic surgeon.

The shape of the RV makes it difficult to analyze geometrically [6]. Although thermodilution has been used successfully to measure RV performance [4] [6] [9], two-dimensional echocardiography has been proven to be a reliable method to assess RV size and function as well [9].

This study was undertaken to confirm echocardiographically the existence of RV dysfunction after major pulmonary resection, to develop hypotheses regarding the mechanisms of the dysfunction and its possible influence on morbidity and mortality.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Patient population
Thirty-one patients undergoing pulmonary resection for primary lung cancer underwent echocardiographic examinations of the RV. The examinations were performed before and 2 days after surgery. The study group (Table 1) consisted of 21 males and 10 females and their ages ranged from 32 to 69 years (mean 59.2 years). None of the patients had symptomatic coronary artery disease, valvular heart disease or arrhythmias. Physical examination and electrocargiogram at rest were unremarkable.


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Table 1. Patients characteristics

 
In twenty-two patients pulmonectomy and in nine lobectomy were performed. Before induction of the anesthesia a catheter was routinely plead by the anesthesiologist at the T4–T6 level for postoperative continuous thoracic epidural analgesia, a wide spectrum antibiotic and micromolecular heparin were administrated prophylactically. All the patients underwent intubation with a double-lumen endotracheal tube. The mediastinal lymph nodes were dissected in all patients. There was no need to resect a part of the diaphragm, pericardium or superior vena cava due to direct invasion of the tumor. After resection chest tubes were placed in the pleural cavity and remained there during the study period.

Echcardiographic examinations
Echocardiographic examinations were performed in all the patients the day before and 2 days after surgery. During the examinations (an `Acuson 128' unit) RV systolic, RV diastolic, and RV stroke volumes as well as RV ejection fraction were estimated.

Right ventricular volumes were calculated by subtracting the entire left ventricle (including the left myocardium) from the entire heart (including the right ventricle and the entire left ventricle [10] [11]. Both the volumes (the entire heart and the entire left ventricle) were calculated as hemiellipsoid by the area-length method with the use of apical four-and two-chamber views [10] [12].

The examinations were standardized. In all cases five cardiac cycles were estimated by two cardiologists.

Statistical analysis
All the results of the measurements were presented as mean±standard deviation and range. Statistical analysis was performed using Student's t-test to compare the results before and after surgery in particular patients. Between-group comparisons were evaluated by Wilcoxon rank sum test. Significance was determined at P<0.05.


    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
No patients died during hospitalization. None of the patients had to be reoperated due to postoperative complications.

The hemodynamic measurements are summarized in Table 2Table 3. Significant elevations in RV end-diastolic and RV end-systolic volumes as well as significant decline in the RV ejection fraction were noted in patients after pneumonectomy. In these patients, RV stroke volume did not change significantly after surgery. No statistically significant changes of any of these parameters were found in patients after lobectomy.


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Table 2. RV hemodynamics parameters before and after pulmonary resection

 

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Table 3. RV hemodynamics parameters before and after pulmonary resection

 
Cardiac arrhythmias occurred in 14 patients after pneumonectomy (63.6%): in seven out of 12 after left pneumonectomy and in seven out of 10 after right pneumonectomy. All the patients developed arrhythmias between the 3rd and the 6th day after surgery and none of them had an intraoperative event of arrhythmia. In the majority of cases (10=71.4%) atrial fibrillation was noted and in four cases (28.6%) supraventricular tachycardiae. None of the patients experiencing arrhythmias died within the hospital stay. In eight cases, recurrent arrhythmias were noted, and three patients were dismissed from the hospital in atrial fibrillation.

The hemodynamic measurements in patients after pneumonectomy with postoperative normal sinus rhythm (group I) and with postoperative supraventricular arrhythmias (group II) were compared and the results are presented in Table 4Table 5. Before surgery the values of RV end-diastolic volume index and RV ejection fraction were similar in patients from the both groups. However, the patients from group II (with subsequent arrhythmias) had much higher RV end-diastolic volume index and lower RV ejection fraction values measured 2 days after surgery (Table 4), although all of them had normal sinus rhythm up to the 3rd postoperative day.


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Table 4. Differences in RV performance parameters in patients with postoperative normal sinus rhythm and supraventricular arrhythmias

 

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Table 5. Right ventricular performance before and after pulmonectomy in patients with and without postoperative supraventricular arrhythmias

 
The changes of RV end-diastolic volume index and RV ejection fraction after pulmonectomy were statistically significant in the both groups and were more expressed in patients with postoperative supraventricular arrhythmias (Table 5).


    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
We have demonstrated echocardiographically that there is a significant dilatation of the RV after pneumonectomy. RV end-diastolic and systolic volumes increased significantly after surgery. We share the opinion presented by other authors [3] [4] [6] that the most likely explanation for this is an increasing right ventricular afterload, secondary to the increase in pulmonary artery pressure and pulmonary vascular resistance after pulmonary resection. The ability of the RV to maintain stroke volume in the face of increased afterload is dependent on the ability to augment end-diastolic volume [4]. Therefore, the size of the RV is revised to maintain output by the Frank–Starling mechanism that improves ejection performance [6] [13]. Until the limited time hemodynamics can be corrected by dilation of the chamber [1] [3] [6] [9]. Our results are similar to those presented in other recent studies [1] [4] [6] [14], in which RV end-diastolic and systolic volumes were significantly increased after pulmonary resection and the differences were most expressed at the 2nd postoperative day [4] [6]. In contrast to these reports however, RV stroke volume index did not change significantly after surgery in our patients. It may indicate that at that time, RV hemodynamics was corrected by dilation. One of the possible explanations for this may be the preoperative condition of the patients (none of them had coronary artery disease, valvular heart disease or arrhythmias).

However, it is known that RV is sensitive to changes in afterload because of its small muscle mass and unlike the left ventricle, the RV is considered to be easily affected by the fluid balance [15] [16]. Enlargement of RV end-diastolic volume increases wall stress by the Laplace relation and augments myocardial oxygen demand, resulting in RV ischemia [4]. Depressed RV contractility may require a marked increase in end-diastolic volume to minimally increase stroke work and ejected volumes. A contractile deficit is one of the factor of the RV dysfunction [4] [6].

In our patients the RV ejection fraction, which represents the pumping potential of the RV was depressed after pneumonectomy. It indicates that the RV myocardial contractility was impaired and it corresponds to other reports [3] [4] [6] [9].

Cardiac arrhythmias are well documented complications that occur after pulmonary resection, with prevalences of 10–22% [4] [7]. The causes of arrhythmias have been contributed to hypoxemia, vagal irrytation, atrial inflammation, preexising cardiac disease and pulmonary hypertension [6]. Surprisingly, we noted cardiac arrhythmias in 14 (64%) of our patients after pneumonectomy. None of them had to have the pericardium resected. These patients however, had much higher RV end-diastolic volume index postoperatively than the patients with normal sinus rhythm.

It is reported that arrhythmias after pneumonectomy may be associated with significant mortality, they occur more frequently after intrapericardial dissection, and in patients in whom postoperative pulmonary edema develops [7]. We suggest that a marked RV distention is a contributory mechanism to development of supraventricular arrhythmias. This distension is easy to detect and may provide the opportunity for interventional therapy. Arrhythmias in our patients were found to be dangerous and they required great efforts to maintain the patients hemodynamisc status. There was no postoperative mortality.

Digitalis administrated prophylactically reduced the incidence of arrhythmias in the next group of our patients, but this problem needs further analysis.

Parallel study of left ventricular function was undertaken retrospectively but the changes of the left ventricular end-diastolic, systolic and stroke volumes as well as the left ventricular ejection fraction after surgery were not statistically significant. In our opinion, more cases are needed to complete the study of the left ventricular function after pulmonary resection.

We have introduced the echocardiographic subtraction method to evaluate the RV performance because this method is not invasive, safe for patients and easy to perform. In addition, a significant correlation was found between RV ejection fraction by thermodilution and two-dimensional echocardiographic fractional area contraction; between RV end-diastolic volume by thermodilution and two-dimensional echocardiographic end-diastolic area; between RV end-systolic volume by thermodilution and two-dimensional echocardiographic end-systolic area [9].

We are aware of the limitations of the echocardiographic subtraction method employed in the study and of the fact that the postoperative evaluation was performed only once. This method is considered to be less accurate than the thermodilution method. Usually larger right ventricular volumes are more underestimated than smaller volumes [10] [12]. It is because generally, it appears to be technically more difficult to record the maximum area of the larger end-diastolic heart than that of the smaller end-systolic heart [10]. That is why we decided to check the results of RV function 48 h after surgery, when the changes are expressed the most [6]. In the next series of our patients, echocardiography is performed 2, 7 and 21 days after surgery and we are satisfied with the usefulness and accuracy of the method.

The results of this study were obtained from a small number of patients and the patients characteristics were heterogeneous (12 had left pneumonectomy, ten right pneumonectomy and nine lobectomies). Therefore, the meaning of the findings is limited and further additional investigations may be necessary.


    Footnotes
 
Presented at the 12th Annual Meeting of the European Association for Cardio-thoracic Surgery, Brussels, Belgium, September 20–23, 1998. Back


    Appendix A. Conference discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Dr P. De Leyn (Leuven, Belgium): Did you compare your right ventricular function after pneumonectomy with the preoperative FEV1 and diffusion capacity? I mean, you probably had patients with a very good lung function before pneumonectomy.

Dr Kowalewski: No, we did not perform such a comparison. In this paper, we concentrated only on the right ventricular morphology and function.

Dr De Leyn: You might expect that, in a group of patients with normal preoperative FEV1, the effect on the right ventricular function would have been less than in the group with poor pulmonary function? You did not analyze this?

Dr Kowalewski: No.

Dr D. Skinner (New York, NY, USA): Did you do pulmonary function preoperatively on all patients?

Dr Kowalewski: Yes, we did, but we did not analyze it in this paper.

Dr J. Hasse (Freiburg, Germany): This is a very nice study. I would like to ask you whether you did adjust your findings to the CVP and whether you have looked at the body weight to estimate whether cardiac index was increased for any reasons? We know about renal dysfunction after large operations, and it could be of interest whether right heart failure may be responsible.

Dr Kowalewski: Any time we present our data, we use indexes. It means that the particular volumes were calculated by dividing with the body surface area. At any time we take into consideration the rate or the body surface area, of course.

Mr H. Gama (Glasgow, UK): In the North America Chest Surgery Clinics from August 1998, they have a paper with similar results where they measured the right ventricular function in terms of dilatation. Also, they measure the pressure in the right ventricle, and they suggest that the increase of pressure in the right side of the heart, after either lobectomy or pneumonectomy, is for them, one of the main factors to development of supraventricular arrhythmias in the post-op.

Dr Kowalewski: Yes, this is true.

Dr P. Macchiarini (Le Plessis-Robinson, France): Looking to your abstract, you start with a right ventricular ejection fraction of 58, but on the slide it is 48?

Dr Kowalewski: Yes, thank you, it should be 48. It's a mistake.

Dr Macchiarini: So I'm a little bit surprised because it's a very low ejection fraction in a surgical population. So do you have any explanation for that?

Dr Kowalewski: You know, if you can see on the direct measurement, for example, thermodilution measurement, the results are usually higher. I think, in my opinion, it's kind of an underestimation because of the method. This method is indirect and perhaps is, frankly speaking, less accurate than the thermodilution method. But we tried to choose a simple, easy to repeat, and triple method to perform.

Dr Macchiarini: The fact that you have a right ventricle dilation in patients with a pneumonectomy doesn't mean that because of the increased pulmonary vascular resistance you have a dilated right ventricle. Therefore, you could speculate that the supraventricular arrhythmias are due to the dilation by itself or eventually by tricuspid regurgitation, if you had any.

Dr Kowalewski: Yes, we have. We had regurgitation. Although, before surgery, we did not see any of these malformations in our patients. But after the dilation, we found these malformations in three or four patients, yes.

Mr J. Khalil-Marzouk (Birmingham, UK): You've conducted your study only once, 2 days after surgery. Why did you not repeat it again, say, a week later, particularly for those who developed arrhythmias?

Dr Kowalewski: It's a very interesting question you ask. In many papers the results of this measurement are most exposed in the second postoperative day. So we decided to make a short study, and we concentrated before and on the second postoperative day. Because in the previous studies, the function of the right ventricle becomes more stable after 1 week, 2 weeks, and after 1 month.

Dr Skinner: You mentioned therapeutic intervention, but you didn't discuss that. Did any of your patients have a digitalis product during the course of surgery? Do you recommend that routinely?

Dr Kowalewski: It's a basic question, yes. Now, we work on a second series of patients and we administer our patients digitalis products prophylactically. So if we found any important distention of the right ventricle, we give them this medicine, even if they present with normal sinus rhythm. Also, we reduce the incidence of arrhythmias, but this is a very short and limited series.

Dr Skinner: Right. But none of these patients you studied had a digitalis problem?

Dr Kowalewski: No.

Mr Dussek: It's a high incidence of arrhythmias with a low ejection fraction preoperatively, as he pointed out. It may correlate.


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 

  1. Nishimura H., Haniuda M., Morimoto M., Kubo K. Cardiopulmonary function after pulmonary lobectomy in patients with lung cancer. Ann Thorac Surg 1993;55:1477-1484.[Abstract]
  2. Lewis J.W., Jr., Gabriel F., Bastanfar M., Servin J. Right ventricular performance in patients undergoing pneumonectomy. Chest 1992;102:63S-67S.
  3. Gill Cryer H., Mavroudis C., Jun Yu., Roberts A.M., Cue J.I., Richardson J.D., Polk H.C. Shock, transfusion and pneumonectomy. Ann Surg 1990;212:197-201.[Medline]
  4. Reed C.E., Spinale F.G., Crawford F.A., Jr. Effect of pulmonary resection on right ventricular function. Ann Thorac Surg 1992;53:578-582.[Abstract]
  5. Okada M., Okada M., Ishi N., Yamashita C., Sugimoto T., Okada K., Yamagishi H., Yamashita T., Matsuda H. Right ventricular ejection fraction in the preoperative risk evaluation of candidates for pulmonary resection. J Thorac Cardiovasc Surg 1996;112:364-370.[Abstract/Free Full Text]
  6. Okada M., Toshiaki O., Okada M., Matsuda H., Okada K., Ishii N. Right ventricular dysfunction after major pulmonary resection. J Thorac Cardiovasc Surg 1994;108:503-511.[Abstract/Free Full Text]
  7. Krowka M.J., Pairolero P.C., Trastek V.F., Payne W.S., Bernatz P.E. Cardiac dysrhythmia following pneumonectomy. Chest 1987;91:490-495.[Abstract/Free Full Text]
  8. Lewis J.W., Jr., Bastanfar M., Gabriel F., Mascha E. Right heart function and prediction of respiratory morbidity in patients undergoing pneumonectomy with moderately severe cardiopulmonary dysfunction. J Thorac Cardiovasc Surg 1994;108:169-175.[Abstract/Free Full Text]
  9. Jardin F., Gueret P., Dubourg O., Farcot J.C., Margairaz A., Bourdarias J.P. Right ventricular volumes by thermodilution in the adult respiratory distress syndrome. Chest 1985;88:34-39.[Abstract/Free Full Text]
  10. Tomida M., Masuda H., Sumi T., Shiraki H., Gotoh K., Yagi Y., Tsukamato T. Estimation of right ventricular volume by modified echocardiographic subtraction method. Am Heart J 1992;123:1011-1022.[Medline]
  11. Levine R.A., Gibson T.C., Aretz T. Echocardiographic measurement of right ventricular volume. Circulation 1984;3:497-505.
  12. Bommer W., Weinter L., Neumann A., Neef J., Mason D.T., DeMaria A. Determination of right atrial and right ventricular size by two-dimensional echocardiography. Circulation 1979;60:91-100.[Abstract/Free Full Text]
  13. Larsen K.R., Svendsen U.G., Milman N., Brenoe J., Petersen B.N. Cardiopulmonary function at rest and during exercise after resection for bronchial carcinoma. Ann Thorac Surg 1997;64:960-964.[Abstract/Free Full Text]
  14. Patel R.L., Townsend E.R., Fountain S.W. Elective pneumonectomy: factors associated with morbidity and operative mortality. Ann Thorac Surg 1992;54:84-88.[Abstract]
  15. Ferguson M.K., Reeder L.B., Mick R. Optimizing selection of patients for major lung resection. J Thorac Cardiovasc Surg 1995;109:275-281.[Abstract/Free Full Text]
  16. Kearney D.J., Lee T.H., Reilly J.J., DeCamp M.M., Sugarbaker D.J. Assessment of preoperative risk in patients undergoing lung resection. Importance of predicted pulmonary function. Chest 1994;105:753-793.



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