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Ann Thorac Surg 1996;62:225-231
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Mechanisms of Right Ventricular Dysfunction After Pulmonary Resection

Divisions of Cardiothoracic Surgery and Anesthesiology, Medical University of South Carolina, Charleston, South Carolina

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. Significant right ventricular (RV) dysfunction as measured by increased end-diastolic volume and reduced ejection fraction has been documented in the postoperative period after pulmonary resection. We hypothesized that changes in RV contractile state or afterload may contribute to this RV pump dysfunction.

Methods. In part one of the study, RV preload was altered on postoperative day 2 (n = 6) by rapid infusion of Hespan to a total of 250, 500, and 1,000 mL. The relationship between RV stroke work and end-diastolic volume was plotted using linear regression. This preload recruitable stroke work relation had been previously validated as a load-insensitive index of RV contractility. The slopes of the preoperative relation (n = 35) and postoperative relation were compared. In part two of the study, RV afterload was reduced by continuous infusion of prostaglandin E₁ (n = 6) through postoperative day 2 and RV pump function was assessed.

Results. Comparison of the slopes of the preload recruitable stroke work relation plotted preoperatively and on postoperative day 2 revealed no significant difference, indicating no change in RV contractile state. Infusion of prostaglandin E₁ in the postoperative period (n = 6) significantly reduced pulmonary vascular resistance (3.67 ± 0.19 versus baseline 5.72 ± 0.19 dyne•s•cm^-5/m²; p < 0.05). However, RV ejection fraction remained significantly reduced (0.34 ± 0.01 versus baseline 0.42 ± 0.01; p < 0.05) and end-diastolic volume significantly increased (105 ± 5 versus baseline 93 ± 2 mL/m²; p < 0.05). Heart rate was increased compared with baseline throughout the postoperative period.

Conclusions. The present study suggests that RV dysfunction after pulmonary resection is not caused by primary alterations in contractility or immediate changes in afterload. Better control of heart rate with minimal effect on inotropy may enhance RV pump function.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
See also page 231.

The study of right ventricular (RV) performance in various disease states has been hampered by the notion that the RV has a relatively unimportant contribution to overall hemodynamic performance and by the inability to easily quantitate RV function secondary to its complex geometry. The development of the RV thermodilution ejection fraction/oximetric catheter has allowed assessment of RV performance in a variety of settings including shock [1], sepsis [2, 3], thermal injury [4], and after coronary artery bypass grafting [5]. Because pulmonary resection has the potential to directly alter RV function, our laboratory first investigated RV performance after major thoracic resection. Significant RV dysfunction as measured by increased RV end-diastolic volume index (RVEDVI) and reduced RV ejection fraction (RVEF) was documented in the postoperative period and appeared to peak on the second postoperative day [6]. Although this RV dysfunction after pulmonary resection has been subsequently confirmed [7], the etiology of the changes in RV performance remains unclear. Appropriate treatment of this postoperative decline in RV function requires a knowledge of the mechanisms involved. Moreover, correction of the RV dysfunction after thoracic resection may result in reduced patient morbidity including a decrease in postoperative complications such as arrhythmias. The purpose of this study, therefore, was to examine potential mechanisms responsible for the deterioration in RV performance after pulmonary resection.

Primary determinants of RV function include preload, afterload, and contractility. Because preload remained unchanged in our original description of postoperative RV function after pulmonary resection, we speculated that alterations in RV contractility or changes in RV afterload may be responsible for the RV dysfunction observed. The slope of the relation between stroke work and end-diastolic length, unaffected by change in either preload or afterload, offered a means to quantitate RV contractile performance. The preload recruitable stroke work relation, constructed by preload volume augmentation, was subsequently validated by us as a load-insensitive index of contractile state [8]. This tool was used in part one of the present study to evaluate alterations in RV contractility on postoperative day (POD) 2 at the peak of RV dysfunction. The administration of prostaglandin E₁ (PGE₁) though a right atrial catheter at low concentrations has been shown to reduce pulmonary vascular resistance with minimal effects on systemic vascular resistance. Therefore, in part two of our study, RV afterload was reduced by constant infusion of PGE₁ through POD 2, and RV function was assessed to evaluate the contribution of changes in afterload to the postoperative decline in RV function observed.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Part One
Right ventricular stroke work, RVEDVI, and RVEF were measured in 35 patients undergoing pulmonary resection (lobectomy or pneumonectomy) preoperatively and postoperatively using a rapid-response pulmonary artery thermistor and thermodilution methods. At the time of operation RV contractile function was assessed by constructing an RV preload recruitable stroke work relation after rapid volume infusion. The techniques of thermodilution measurements and alteration of RV preload have previously been documented [6, 8]. Briefly, a rapid-response thermistor (7.5F; Baxter Healthcare Corp, Irvine, CA) was inserted via the right internal jugular vein and positioned 4 cm distal to the pulmonary valve. Using this catheter and computer system, RVEF, cardiac output, and RV volumes were computed. Right ventricular stroke volume was computed as the quotient of cardiac output and heart rate. Right ventricular end-diastolic volume and RV end-systolic volume were subsequently computed from RV stroke volume and RVEF measurements. Cardiac output and RV volumes were indexed to the patient's body surface area. After a stabilization period in the operating room, baseline hemodynamic and RV function measurements were obtained. Right ventricular preload was then serially increased by the rapid infusion of Hespan (DuPont Pharmaceuticals, Wilmington, DE) to a total of 250 mL, 500 mL, and 1,000 mL. Right ventricular thermodilution and hemodynamic measurements were repeated after each infusion and again at 4 to 6 hours, 24 hours, and 48 hours postoperatively.

In 6 patients, RV contractile function was reassessed at 48 hours postoperatively by reconstructing an RV preload recruitable stroke work relation by the rapid volume infusion of Hespan to a total of 250 mL, 500 mL and 1,000 mL. The relationship between RV stroke work and RV end-diastolic volume, the preload recruitable stroke work relation, was examined in the preoperative and postoperative periods using linear regression analysis.

Part Two
Ten patients undergoing lobectomy were included in this study. The multilumen thermodilution catheter was inserted as previously described and used to measure hemodynamic parameters including pulmonary artery pressure, central venous pressure, pulmonary capillary wedge pressure, cardiac output, RVEF, RV stroke volume, RV end-diastolic volume, and RV end-systolic volume. Using simultaneously obtained hemodynamic and thermodilution measurements, pulmonary vascular resistance, systemic vascular resistance, and stroke work were computed and normalized to the patient's body surface area.

After collection of baseline data, the patient's pulmonary capillary wedge pressure was increased by rapid intravenous volume infusions of Hespan to a total of 250 mL, 500 mL and 1,000 mL, and hemodynamic data were collected after each volume infusion. To establish a preoperative RV function curve at different RV afterload values, PGE₁ (donated by Upjohn Co, Kalamazoo, MI) was then infused through the right atrial catheter at 0.025, 0.05, and 0.1 µg•kg^-1•min^-1 with hemodynamic and RV function data collected after 10 minutes of stabilization at each rate. The infusion rate was then decreased to 0.05 µg•kg^-1•min^-1 for the duration of the operation and for the initial 48 hours postoperatively in 6 patients. Hemodynamic and thermodilution measurements were collected at 6, 24, and 48 hours after operation. The ventricular function curve using different RV afterload values was repeated on POD 2 by reducing the PGE₁ infusion to 0.025 µg•kg^-1•min^-1 and finally repeating the data collection without PGE₁. No other vasodilator therapy was used during the postoperative period.

The relationship between changes in RV afterload and changes in RVEF was examined preoperatively and at 48 hours postoperatively. The changes in loading conditions of the RV secondary to PGE₁ infusion were examined in relation to RV performance to determine if there was improvement in RV pump function after a reduction in RV afterload.

Patient Population
All patients underwent thoracotomy for the resection of lung cancer at the Medical University of South Carolina, Charleston, SC. No patient had a prior history of myocardial infarction, chronic arrhythmia, pulmonary hypertension, or severe obstructive or restrictive lung disease (forced vital capacity less than 50% of predicted or forced expiratory volume in 1 second less than 50% of predicted). Consent was obtained according to the guidelines of the Human Institutional Review Board.

Statistical Analysis
Hemodynamic measurements and indices of RV function were compared at various time points using multiway analysis of variance. Pairwise tests of individual group means were compared using the paired t test. The relationship between RV end-diastolic volume and RV stroke work during volume loading and during incremental PGE₁ infusion were examined using linear regression analysis. From this analysis, the regression equation and confidence intervals for the RV preload recruitable stroke work relation were obtained. Results are presented as mean ± standard error of the mean. Values of p less than 0.05 were considered statistically significant.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Part One
A summary of hemodynamics and RV pump function parameters from the time of operation throughout POD 2 in 35 patients is shown in Table 1. Right ventricular dysfunction is again confirmed on POD 2 by the significant increase in RVEDVI and decrease in RVEF. In 6 patients preload augmentation (rapid infusion to a total of 250, 500, and 1,000 mL of Hespan) was repeated on POD 2 (Table 2). Indices of RV function were repeated after each bolus of Hespan, and the relationship of RV stroke work to end-diastolic volume was plotted using linear regression. This preload recruitable stroke work relation was highly linear: RV stroke volume index = 0.30 (RVEDVI) - 21 (r = 0.98) (Fig 1). The POD 2 relation was compared with that constructed in the preoperative period: RV stroke volume index = 0.38 (RVEDVI) - 25 (r = 0.98). As shown in Figure 1, the slopes of these preload recruitable stroke work relations were not significantly different, which suggests no change in RV contractile state.

View larger version (16K): [in this window] [in a new window]   Fig 1. . Right ventricular (RV) function curves were obtained with preload augmentation of Hespan infused to a total of 250, 500, and 1,000 mL. Plotting the values for RV end-diastolic volume (x-axis) and RV stroke work (y-axis) yields the preload recruitable stroke work relation. This relationship was determined preoperatively and on postoperative day 2 and subjected to regression analysis. There was no significant difference in the slope obtained preoperatively and postoperatively, suggesting that RV contractile function was unchanged.

View larger version (16K): [in this window] [in a new window]   Fig 2. . After preoperative volume loading with 1,000 mL of Hespan, prostaglandin E1 (PGE1) was successfully infused at doses of 0.025, 0.05, and 0.10 µg•kg-1•min-1. After stabilization, right ventricular (RV) measurements were obtained. Pulmonary vascular resistance (PVRI) and RV ejection fraction (RVEF) were plotted against PGE1 dose. Pulmonary vascular resistance decreased in a nonlinear fashion with no change in RVEF. Despite postoperative infusion of PGE1 and reduced PVRI resistance on postoperative day (POD) 2, RVEF was significantly decreased from its preoperative value (p < 0.05).

View larger version (14K): [in this window] [in a new window]   Fig 3. . Effect of prostaglandin E1 infusion in the postoperative period is shown compared with preoperative baseline values. Right ventricular ejection fraction (RVEF) remained significantly reduced and right ventricular end-diastolic volume (RVEDVI) remained increased on postoperative days 1 and 2 compared with baseline (p < 0.05) despite constant prostaglandin E1 infusion. Heart rate (HR) was significantly elevated throughout the postoperative period (p < 0.05 compared with baseline).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

Prostaglandin E₁ was used in the present study to cause pulmonary vasodilatation and thereby reduce pulmonary vascular resistance. Pulmonary vasodilatation by PGE₁ has been reported in patients with mitral valve disease, primary pulmonary hypertension, and decompensated chronic obstructive lung disease, and in patients after cardiac transplantation [9–14]. The recommended dose of PGE₁ ranges from 0.025 to 0.20 µg•kg^-1•min^-1 [15]. At low concentrations, more than 90% of PGE₁ is cleared during the first pass through the pulmonary vasculature, which can minimize any systemic effect and negate the need for systemic afterload support [16]. In the present study a low-dose infusion of PGE₁ effectively reduced pulmonary vascular resistance index and pulmonary artery pressures throughout the first 2 postoperative days without any requirement for afterload support of the systemic circulation. Increasing the dose of PGE₁ infusion resulted in little decrease in pulmonary vascular resistance but did result in significant reductions in systemic blood pressure. Our results suggest that 0.025 µg•kg^-1•min^-1 represents an optimal PGE₁ infusion rate after lobectomy to effect a reduction in pulmonary vascular resistance without causing significant changes in the systemic circulation.

In contrast to the left ventricle, RV pump performance rapidly declines with increased afterload [17, 18]. For example, Abel and Waldhausen [18] demonstrated that a rapid linear fall in RV stroke volume occurred with pulmonary artery constriction in dogs. In the present study, a prostaglandin infusion was administered in patients after pulmonary resection to determine whether a reduction in RV afterload would remove, at least in part, the RV pump dysfunction that had occurred. Although prostaglandin infusion significantly reduced pulmonary vascular resistance, a significant improvement in RV pump function was not achieved. These findings suggest that a contributory factor for the RV dilatation and pump dysfunction that occurs after pulmonary resection is not due to changes in RV afterload. However, there are limitations to this portion of the present study that must be recognized. Postoperative RV function measurements with prostaglandin infusion were performed when heart rate was significantly increased compared with baseline and compared with measurements without PGE₁ infusion. Mean arterial pressure was reduced in the postoperative period to a similar degree both in patients with and without PGE₁. An important determinant of coronary blood flow is perfusion pressure and the duration of diastole [19]. Thus, the alterations in arterial pressure and heart rate that occurred may have influenced right coronary flow and therefore RV function. In the present study, RV preload recruitable stroke work was not determined in patients with simultaneous prostaglandin infusion. Thus, it remains unknown whether RV contractile performance was affected by prostaglandin infusion, which, in turn, may have confounded the RV pump function measurements. In light of these limitations, the findings from the present study cannot completely exclude the possibility that changes in RV afterload may occur after pulmonary resection and thereby influence RV pump performance. Future studies that examine RV pump function in patients after pulmonary resection in which RV afterload reduction is achieved in the absence of systemic effects would be appropriate.

In the present study, RV contractile function was assessed by the preload recruitable stroke work relation [8] 2 days after pulmonary resection and compared with preoperative, baseline values. The slope of this relation, which is an index of RV contractile performance [20–22], was unchanged. This observation would suggest that the reduced RVEF observed postoperatively after pulmonary resection was not due to an inherent defect in RV contractile performance. It must be recognized that in the present study, baseline RV contractile performance was assessed intraoperatively under sedation whereas RV contractile function was measured postoperatively in the conscious patient. These different conditions are an important consideration when making comparisons of the RV preload recruitable stroke work relation. Nevertheless, in these same patients, there was no change in the slope of the RV preload recruitable stroke work relation despite a significant fall in RVEF.

A potential contributory factor for the maintenance of RV contractile performance despite the significant change in RV pump function in this early postoperative period is heightened sympathetic tone. Increased levels of circulating catecholamines may occur in patients after pulmonary resection due to postthoracotomy pain or other systemic influences [22, 23]. Additional evidence to suggest that heightened sympathetic tone was present in patients 2 days after pulmonary resection was the significantly increased heart rate. Indeed, the increased resting heart rate may have contributed to the RV dilatation and reduced pump function that were observed in the present study. Right ventricular ejection into the pulmonary circuit is based on a peristaltic motion that is generated at the RV apex and then moves into the narrowed infundibular region [17]. Thus, the time-dependent changes in RV geometry during the contraction period significantly influence overall stroke volume. Right ventricular regional and global performance is significantly influenced by changes in myocardial activation periods [24, 25]. For example, Lancon and colleagues [25] reported that increasing the basal resting heart rate in patients from 73 to 100 beats/min diminished RV preload-dependent stroke volume without a significant change in RV contractile performance. Interestingly, in the present study, the fall in RVEF observed in patients 2 days after pulmonary resection was accompanied by a similar increase in heart rate, with no apparent change in RV contractile state. Thus, one contributory mechanism for the RV dilatation and reduced ejection performance that was observed in patients after pulmonary resection is diminished RV ejection efficiency due to increased heart rate. This issue could be examined through the use of ß-adrenergic receptor antagonists at a dosage regimen that would reduce heart rate but have minimal effects on contractile function. Through this approach, the reduction in heart rate would prolong the RV ejection period and therefore increase RV output. In light of the findings from the present study, the specific chronotropic effects on RV geometry and pump function after pulmonary resection warrant further investigation.

The present study demonstrated that increased afterload probably does not contribute to the reduced pump function postoperatively. Okada and associates [7] and past reports from our laboratory [6, 8] demonstrated that mean pulmonary artery pressures and pulmonary vascular resistance remained unchanged on POD 2. Okada and associates [7] reported significant elevations in pulmonary arterial pressure and pulmonary vascular resistance index during exercise in the third postoperative week after resection. They hypothesized that changes in RV afterload were the main determinants of the postoperative deterioration of RV pump performance, and that RV dilatation masked this change by serving as a "reservoir." Thus, increased RV afterload may become an important determinant of RV pump function later in the postoperative course. Our studies included only a few patients undergoing pneumonectomy, and only lobectomy patients underwent postoperative preload augmentation or PGE₁ infusion. Because 50% of the pulmonary vascular bed is removed by pneumonectomy, a source of RV dysfunction may indeed be increased RV afterload in this group. Okada and associates [7] noted an association between atrial fibrillation and increased RV end-diastolic volumes. The incidence of arrhythmias, predominantly supraventricular tachycardias, is 25% after lobectomy and even higher after pneumonectomy [26]. The cause remains unclear. We noted that the development of atrial fibrillation tended to be more common in patients with greater postoperative dilatation. However, a larger number of patients will be required to analyze the group of patients in whom postoperative arrhythmias or pulmonary edema develop.

In summary, for patients with demonstrated significant elevation of mean pulmonary artery pressure or pulmonary vascular resistance, a low-dose constant infusion of PGE₁ (0.025 µg•kg^-1•min^-1) can be safely administered with a significant decrease in pulmonary afterload. The present study suggests that RV dysfunction after pulmonary resection is not caused by primary alterations in contractility or immediate changes in afterload. Better control of heart rate with minimal effect on inotropy may enhance RV pump function.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
This work was supported in part by National Institutes of Health grant HL-45024 (F.G.S.), an American Heart Association Grant-in-Aid (F.G.S.), American Heart Association, South Carolina Affiliate (B.H.D.), and South Carolina American Lung Association (C.E.R.). Doctor Spinale is an Established Investigator of the American Heart Association.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.

Address correspondence to Dr Reed, Division of Cardiothoracic Surgery, Medical University of South Carolina, 171 Ashley Ave, Charleston, SC 29425.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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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): Carolyn E. Reed Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Reed, C. E. Articles by Spinale, F. G. Search for Related Content PubMed PubMed Citation Articles by Reed, C. E. Articles by Spinale, F. G. Related Collections Related Article