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J Thorac Cardiovasc Surg 1994;108:503-511
© 1994 Mosby, Inc.

GENERAL THORACIC SURGERY

Right ventricular dysfunction after major pulmonary resection

Kobe, Japan

From the Department of Surgery, Division II, Kobe University School of Medicine, Kobe, Japan.

Received for publication Nov. 2, 1993. Accepted for publication Feb. 4, 1994. Address for reprints: Morihito Okada, MD, Department of Surgery, Division II, Kobe University School of Medicine, Kusunoki-cho 7-5-2, Chuo-ku, Kobe, 650 Japan.

Abstract

Right ventricular performance was assessed by thermodilution in 20 patients at rest and during exercise before and after lobectomy or pneumonectomy. The right ventricular ejection fraction was significantly decreased on the first postoperative day (0.36±0.34), the second postoperative day (0.34±0.04), and the third postoperative week (0.37±0.06) relative to the preoperative right ventricular ejection fraction value (0.43±0.07, p < 0.05). The right ventricular end-diastolic volume index was significantly increased by the second postoperative day (130±24 ml/m²) compared with the preoperative value (112±20 ml/m²). A significant decrease in the right ventricular stroke volume index was observed after operation, with a significant increase in heart rate considered necessary to maintain cardiac output. Pulmonary arterial pressure, the pulmonary vascular resistance index, and central venous pressure were unaltered over time. Indices of left ventricular function (that is, cardiac index, arterial pressure, and pulmonary arterial wedge pressure) were also preserved throughout the postoperative period. To explain the right ventricular dysfunction, ergometric exercise values were compared and the heart rate, pulmonary arterial pressure, central venous pressure, pulmonary vascular resistance index, and right ventricular end-diastolic volume index were all higher and the right ventricular ejection fraction lower during exercise after the operation. However, indices of left ventricular function remained unchanged. Significant elevations in pulmonary arterial pressure and the pulmonary vascular resistance index only during exercise occurred. These findings indicate that changes in right ventricular function at rest compensate for the increase in right ventricular volume, but adequate compensation does not occur during exercise, with a resultant increase in pulmonary arterial pressure and the pulmonary vascular resistance index. This suggests that a change in afterload may be the main determinant of the deterioration in right ventricular pump performance during exercise. We speculate that the main cause of right ventricular dysfunction after major pulmonary resection might be the changes in right ventricular afterload. The right ventricle may play an important role serving as a"reservoir"for afterload. (J THORAC CARDIOVASC SURG 1994;108:503-11)

Although right ventricular (RV) function has been shown to be important in serious diseases, ^1-3 only limited information on RV adaptation to pulmonary resection has been reported. The relative neglect of RV performance in clinical and laboratory investigations has resulted in part from the focus on the left ventricle as the most important chamber of the heart. The shape of the RV makes it difficult to analyze geometrically. Recently, thermodilution has been used successfully to measure RV performance. Several clinical studies have demonstrated the utility of this method for monitoring RV function in critically ill patients. ^4,5 Additionally, the thermodilution method allows us to assess RV function during exercise and at rest.

The complications that follow thoracic operations may be associated with an increased mortality. Cardiac arrhythmias are cases in point. The causes of these complications require further clarification, although several factors are likely to be involved. We hypothesize that RV dysfunction is a problem when the effects of pulmonary resection and its complications are dealt with. Therefore this study was undertaken to confirm the existence of RV dysfunction after major pulmonary resection and to determine its degree and duration. The overall goal of this project was to determine the causes of RV dysfunction.

PATIENTS AND METHODS

Patient population
The study included 20 patients with primary lung cancer who had undergone either pneumonectomy or lobectomy. Ten patients had studies of the RV done during exercise as well as at rest. Informed consent to take part in the study was obtained from all patients.

Eighteen men and two women with a mean age of 62 years (range 49 to 77 years) composed the patient population. Procedures included six right upper lobectomies, four left lower lobectomies, three left pneumonectomies, three left upper lobectomies, two right middle and lower lobectomies, and two right lower lobectomies. The mediastinal lymph nodes were dissected in all patients. All patients underwent placement of an RV thermodilution ejection fraction/volumetric catheter, insertion of radial arterial catheters for blood pressure monitoring, and intubation with a double-lumen endotracheal tube that was maintained only during the operation. Chest tubes were placed in the pleural cavity for more than 2 days after the procedure and remained at -15 cm H₂O suction. No patient had prior clinical evidence of coronary artery disease, valvular heart disease, hypertension, or arrhythmias. None of the patients had a significant medical history or received any cardiopulmonary medications. Physical examination and electrocardiogram at rest were unremarkable. We have previously reported that tricuspid valve regurgitation might create significant errors in RV thermodilution ejection fraction measurements ⁶; however, apparent tricuspid regurgitation was not found in any of the patients. Most of the patients had obstructive or restrictive lung disease with 1.78 ± 0.20 L of forced expiratory volume in 1 second and an average forced vital capacity of 2.81 ± 0.15 L.

Exercise protocol
In the final 10 subjects, a single-stage, submaximal exercise protocol was used. This approach provided relatively steady-state, aerobic exercise conditions. Baseline parameters were measured after a 10-minute rest in the supine position. The exercise tests were done in the supine position on a bicycle ergometer with a changeless work load of 80 watts for 5 minutes. The patients began pedaling at a constant rate of approximately 65 rpm. During exercise, the lower limbs were elevated with the pedal axis located 30 cm higher than the table level. Measurements were obtained after 5 minutes of constant exercise at each effort level.

Measurements
Parameters were measured with a cardiac monitor for heart rate (HR) and with a manometer for the measurement of direct brachial arterial pressure. An iced (3° C) 5 ml bolus of 5% dextrose was injected into the right atrium over 1.5 seconds. A multilumen 7.5F catheter mounted with a rapid-response thermistor (Baxter Healthcare Corp., Irvine, Calif.) was positioned 3 cm distal to the pulmonary valve to measure the thermodilution signal. This was interfaced to a thermodilution ejection fraction computer (REF-1; Baxter Healthcare Corp.). The cardiac output was calculated from the thermodilution curve as has been previously described. ^7,8 In addition to cardiac output, the RV ejection fraction was computed by the thermodilution method as has been previously described. ^9,10 This method obviates the need for geometric assumptions of RV shape and does not necessitate the use of complex equipment. The thermodilution method depends on temperature changes that occur in the pulmonary artery for ejection fraction measurements. The RV end-diastolic volume was calculated as a quotient of the RV stroke volume (cardiac output/HR) and the RV ejection fraction. The other parameters measured were arterial pressure, central venous pressure, pulmonary artery pressure (PAP), and the pulmonary capillary wedge pressure. These measurements at rest were reported before induction of anesthesia, 1 hour after transport to the intensive care unit, 6 hours after operation, on the first postoperative day, on the second postoperative day, and during the third postoperative week. They were taken under stable conditions during spontaneous ventilation.

Statistical analysis
Hemodynamic measurements and indices of cardiac function were compared at the various times by multiway analysis of variance. Differences at each time were tested by the paired t test. When the F ratio of the analysis of variance was significant (p < 0.05), the differences were tested by Scheffe F test. All data in the text, tables, and figures are presented as the mean plus or minus the standard deviation.

RESULTS

There was no operative mortality. No patients had major complications with the exception of sustained atrial fibrillation in three patients who each had a relative rise in the RV end-diastolic volume index and RV end-systolic volume index over time. The hemodynamic measurements at rest and during exercise are summarized in Tables I and II.

HR at rest rose significantly in the early postoperative period compared with the preoperative HRs. However, by the third postoperative week, postoperative and preoperative HRs did not significantly differ. HR during exercise was significantly higher after operation (Fig. 1). Although arterial pressure, pulmonary capillary wedge pressure, central venous pressure, and the cardiac index at rest were unchanged over time, a significant drop in arterial pressure and elevation in central venous pressure were noticed during exercise. PAP did not change at rest, but after operation it significantly increased during exercise (Fig. 2). The PVR index at rest tended to decrease gradually in the early postoperative period, but returned to the preoperative value by the third postoperative week. During exercise, the postoperative PVR indices, like PAPs, increased significantly (Fig. 3). Although at rest PAP and the PVR index remained unchanged or only slightly decreased, the RV ejection fraction was significantly decreased by the second postoperative day with no return to baseline levels. Likewise, the RV ejection fraction decreased significantly after operation during exercise (Fig. 4). In the early postoperative period, the RV end-diastolic volume index at rest gradually increased, reaching a significant point on the second postoperative day. It later returned to the preoperative value by the third postoperative week. The postoperative RV end-diastolic volume indices during exercise were significantly higher than preoperative RV end-diastolic volume indices (Fig. 5).

View larger version (16K): [in this window] [in a new window]   Fig. 1. HR at rest increased significantly from early postoperative hours to second postoperative day compared with preoperative values (p < 0.05). However, by third postoperative week, HR had returned to preoperative baseline level. During exercise, there was significant sustained elevation of HR after operation (p < 0.05).

View larger version (17K): [in this window] [in a new window]   Fig. 2. Systolic PAP perioperatively remained unchanged at rest, but postoperative values were significantly higher than preoperative values during exercise (p < 0.05).

View larger version (20K): [in this window] [in a new window]   Fig. 3. PVR index at rest initially decreased, then returned to baseline levels; however, postoperative values rose significantly during exercise (p < 0.05).

View larger version (17K): [in this window] [in a new window]   Fig. 4. RV ejection fraction was significantly decreased in postoperative period when compared with preoperative values obtained both at rest and during exercise (p < 0.05).

View larger version (18K): [in this window] [in a new window]   Fig. 5. RV end-diastolic volume index at rest increased significantly by second postoperative day compared with preoperative value. However, it returned to preoperative value by third postoperative week (p < 0.05). Postoperative values during exercise were significantly higher than preoperative values (p < 0.05).

The relationship between resting and exercise cardiac indices and mean PAPs in our study is shown in Fig. 6. The postoperative flow-pressure curves become steeper when compared with the preoperative curves. The changes in measurements before and after operation did not correlate with resected volumes of lung.

View larger version (34K): [in this window] [in a new window]   Fig. 6. Relationship between resting and exercise cardiac indices and mean PAP values was studied. Slopes of postoperative pressure-flow curves are steeper compared with slopes of preoperative pressure-flow curves.

In early studies it has been implied that the RV plays only a minor role in the loss of initiative for sustaining cardiac output. ¹¹ However, later studies have suggested that the performance of the RV is important in cardiac function under various stresses. ¹² Changes in PAP and PVR influence afterload on the RV. Consequently, the size of the RV may be revised to maintain output by the Frank-Starling mechanism that allows the wall stress to normalize and improves ejection performance. ¹³ Even when myocardial contractility is damaged, hemodynamics can be corrected by dilation of the chamber. ^12,13

In our study, the RV ejection fraction, which represents the pumping potential of the RV, was apparently depressed after major pulmonary resection. The major cause of this depression was originally thought to be an augmentation of RV afterload caused by a rise in PAP and PVR. However, PAP and PVR remained unchanged at rest throughout the postoperative period. The CI, arterial pressure, and pulmonary capillary wedge pressure, which are indices of left ventricular performance, were preserved over time. Unlike the left ventricle, the RV was considered to be easily affected by the fluid balance. Therefore we kept the infusion volume as equal and the hemodynamics as stable as possible. In consequence, central venous pressure, a representation of RV preload, was unchanged in this series. The results of our study in which the RV ejection fraction and the stroke volume index were significantly decreased whereas HR, the RV end-diastolic volume index, and the RV end-systolic volume index were significantly increased were clearly indicative of RV dysfunction. Under normal circumstances, it would be possible for an increase in ventricular volume to lead to an increase in stroke volume by the Frank-Starling mechanism. We have wondered what might be the origin of this RV dysfunction. For this reason we investigated the effects of exercise tolerance, which might be depressed after lung resection because of the development of pulmonary hypertension but which might not be evident at rest.

Cardiac arrhythmias are documented complications that occur after thoracic operation, with prevalences of 10% and 22%. ^14-16 The causes of these arrhythmias have been attributed to hypoxemia, vagal irritation, atrial inflammation, preexisting cardiac disease, and pulmonary hypertension. However, few of these factors have been identified and are generally accepted. Krowka and associates ¹⁴ reported that arrhythmias after pneumonectomy may be associated with significant mortality, have poor correlations with preoperative pulmonary function, and occur more frequently after intrapericardial dissection and in patients in whom postoperative pulmonary edema develops. In our study, approximately 15% of the patients had atrial fibrillation in the postoperative period, and these patients had much higher RV end-diastolic volume index and lower RV ejection fraction values measured before operation both at rest and during exercise. Unfortunately, we were unable to make a statistical comparison of these patients with arrhythmogenesis, because their numbers were too small. We are interested in the relationship between RV dysfunction in terms of RV dilation and pulmonary edema, which yields the greatest mortality after pneumonectomies. We are now studying the effect of resected pulmonary volume on RV function and the further influence of RV dysfunction on the occurrence of atrial arrythmias. We are planning additional studies in which the number of pneumonectomies will allow us to make a statistical analysis to reach more definite conclusions.

Mossberg, Björk, and Holmgren ¹⁷ have demonstrated diminished stroke volume after pneumonectomy caused by impaired filling of the left ventricle secondary to reduced pulmonary blood volume. Despite this decreased stroke volume associated with the reduced pulmonary vascular bed, cardiac output was considered to be maintained by a corresponding increase in HR. Under normal conditions, the pulmonary vasculature applies low resistance to RV outflow, with only about one tenth of the resistance to flow applied by the systemic vascular bed. ¹³ Increased output from the right side of the heart is accommodated by recruitment of previously nonperfused vessels in the more dependent portions of the lung. ¹³ Normally, the RV is not pressure-overloaded because the pulmonary vascular bed reacts to wide variations in blood flow without much change in pressure. Under the situation after major pulmonary resection, at rest, additional pulmonary vasculature is recruited and the RV dilates without an elevation in PAP. However, during exercise, RV cannot accommodate the high intracavitary pressures induced by increases in PAP and PVR and consequently the right-sided heart dysfunction and cor pulmonale develop. This mechanism is well illustrated by the changes in exercise/rest values from preoperative to postoperative examinations, as shown in Table III of our study. Significant elevations were noticed in the exercise/rest values of PAP and PVR index after operation, whereas the RV end-diastolic volume index, the RV end-systolic volume index, and the cardiac index remained relatively unchanged. These findings suggest that before pulmonary resection, changes in cardiac work with exercise loading, in an effort to preserve output, comprise increases in RV volume. After pulmonary resection with resulting RV dysfunction, the increase in RV volume reaches its limits with the resultant rises in PAP and PVR index. Even a small augmentation in cardiac output, or pulmonary blood flow, which occurs with exercise loading, causes a large increase in PAP in patients with restricted pulmonary vascular beds. Mahler and associates ¹⁸ studied the relationship between cardiac index and PAP during exercise in patients with chronic obstructive pulmonary disease. They concluded that elevated RV afterload may be the major factor that depresses RV function. This conclusion was based on results in patients with chronic obstructive pulmonary disease who had inordinate rises in PAP plotted against cardiac index with exercise and who with exercise showed additional elevation in PVR rather than the usual decrease. We thought that the same conclusions might apply to the situation after major pulmonary resection and that the relation of PAP to cardiac index reflects the faculty of pulmonary vasculature. This supposition was confirmed by the relationship between cardiac index and mean PAP from resting to exercise shown in Fig. 6. The postoperative flow-pressure curves rose more steeply as compared with the preoperative ones.

The quality of life after operation is thought to be influenced by the degree of RV dysfunction in maintaining pulmonary blood flow, because PAP sets the limit for increasing flow with exercise. Under the circumstance of the reduced pulmonary vascular bed resulting from pulmonary resection, exercise loading increases the oxygen demand of the body and consequently attempts to augment the cardiac output; however, it is not possible any longer to adapt this requirement satisfactorily. Despite this flow reduction, the blood flow per unit of the remaining lung increases, particularly during exercise, resulting in no change in cardiac index. The expansiveness of the remaining pulmonary vasculature after extensive pulmonary resection has been reported to be restricted compared with that of normal vasculature. ¹⁹ The preceding statements support our findings that significant elevations in PAP and PVR occur during exercise, although there are no changes in these parameters at rest. This suggests that a change in afterload may be the main determinant of the deterioration in RV pump performance, which remains unchanged at rest. Our impression is that the RV may serve as a "reservoir" for afterload, masking the increases in PAP and PVR with its dilation at rest. However, exercise-loading pushes the RV to its limitations, unmasking a clear elevation in afterload.

Finally, it is essential for surgeons to understand the mechanisms that cause RV dysfunction after pulmonary resection. We conclude that a definitive study of RV dysfunction with the use of thermodilution techniques is warranted given the findings of this preliminary work.

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This Article Abstract 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): Masayoshi Okada Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Okada, M. Articles by Ishii, N. Search for Related Content PubMed PubMed Citation Articles by Okada, M. Articles by Ishii, N.