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Ann Thorac Surg 1996;61:516-520
© 1996 The Society of Thoracic Surgeons

Original Article: General Thoracic

Value of Perioperative Doppler Echocardiography in Patients Undergoing Major Lung Resection

David Amar, MD, Michael E. Burt, MD, PhD, Nancy Roistacher, MD, Ruth A. Reinsel, PhD, Robert J. Ginsberg, MD, Roger S. Wilson, MD

Departments of Anesthesiology and Critical Care Medicine, Medicine, and Surgery, Memorial Sloan-Kettering Cancer Center and Cornell University Medical College, New York, New York

Accepted for publication September 21, 1995.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The effects of major lung resection on right heart function have not been well established. Our goal was to evaluate these effects using serial Doppler echocardiography in the perioperative period.

Methods. In 86 patients undergoing lobectomy (n = 47) and pneumonectomy (n = 39), we examined the effects of pulmonary resection on perioperative changes in right heart function by transthoracic echocardiography. Serial echocardiograms were performed preoperatively, on postoperative day 1, and again between postoperative days 2 and 6 (median, 3 days) to evaluate cardiovascular function and to estimate right ventricular systolic pressure by the tricuspid regurgitation jet Doppler velocity method.

Results. Right or left atrial size, right atrial pressure, and estimated right ventricular systolic pressure did not differ between groups on the preoperative or postoperative day 1 examinations. However, on postoperative days 2 through 6 patients who underwent pneumonectomy had higher (mean ± standard deviation) right ventricular systolic pressure values than lobectomy patients (31 ± 15 versus 25 ± 10 mm Hg, respectively; p < 0.05 by analysis of variance). In the subset of patients with percent predicted forced expiratory volume in 1 second less than 60% undergoing pneumonectomy (9/39), preoperative right ventricular systolic pressure was inversely correlated with percent predicted forced expiratory volume in 1 second values (r = -0.78; p < 0.04). This correlation was not significant in corresponding lobectomy patients. Postoperative right ventricular enlargement determined by echocardiography occurred with similar frequency in both groups and was associated with poor short-term prognosis in patients in whom severe respiratory failure developed.

Conclusions. Preoperative indices of right heart function were within the normal range in both groups. Pneumonectomy but not lobectomy was associated with mild postoperative pulmonary hypertension that was not accompanied by significant right ventricular systolic dysfunction. Postoperative echocardiography may be useful to evaluate right heart function in critically ill patients after lung resection.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Concerns of right ventricular dysfunction and altered pulmonary vascular tone after pulmonary resection have been raised but have not been well established in the literature. Such alterations in right heart function could significantly affect the clinical management of these patients in the perioperative period. Despite efforts to evaluate the effects of lung resection on the pulmonary circulation [1] and right heart function [2–4] these studies employed small numbers of patients, with few undergoing pneumonectomy, and lacked the ability to describe the effects of varying degrees of chronic obstructive pulmonary disease (COPD) on these parameters. The lack of enthusiasm for preoperative right heart catheterization for perioperative risk stratification in this patient population is due to its unproven benefit along with the cost and invasive nature of the procedure. Doppler echocardiography has been validated as a noninvasive method to evaluate cardiac function and to estimate right ventricular systolic pressure (RVSP) in a variety of clinical settings and in patients with COPD [5, 6]. The aim of this study was to determine the potential clinical usefulness of measuring RVSP by serial Doppler echocardiography in a representative group of patients undergoing major pulmonary resection with varying impairment of lung function and to determine whether pneumonectomy was associated with greater alterations of right ventricular performance than lobectomy in the critical early postoperative period.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Population
As part of a larger effort to prospectively study the etiology of dysrhythmias after thoracic operations [7], we independently examined the effects of lobectomy and pneumonectomy on indices of right heart function. Written informed consent was obtained from each patient scheduled for major pulmonary resection for malignancy with approval of the Institutional Review Board of Memorial Sloan-Kettering Cancer Center. Excluded were patients undergoing diagnostic or limited (wedge) procedures, those not in sinus rhythm, and patients with a history of prior thoracic operation. Preoperative evaluation consisted of routine blood tests, 12-lead electrocardiogram, and pulmonary function testing. A standard nomogram [8] adjusting for sex, age, and height was used to calculate the percent of predicted values of the forced expired volume in 1 second (FEV1 % pred) and forced vital capacity in all patients. To determine the effect of pulmonary function impairment on right heart function, patients with moderate to severe COPD were defined by an FEV1 % pred less than 60%.

Echocardiography
All patients had awake supine transthoracic echocardiograms performed before operation using a 2.5/2.0-MHz transducer for imaging and Doppler echocardiography (SONOS 1500; Hewlett Packard, Waltham, MA). Subsequent echocardiograms were performed on all patients on the morning of the first postoperative day and once again between postoperative days 2 and 6 (most commonly on postoperative day 3). All patients were in sinus rhythm at the time echocardiography was performed. Any evidence of pericardial disease and serial changes in right or left ventricular size were recorded. Abnormal left ventricular function was defined by an ejection fraction less than 0.50. Right and left atrial superior-to-inferior diameters were measured in the apical four-chamber view at end-systole from still frames. The apical four-chamber, parasternal, and the subxiphoid views were used to access the maximum tricuspid regurgitation jet (TRJ) Doppler velocity. The regurgitant jet was localized in the pulsed mode, then maximized and measured in the continuous wave mode at a sweep speed of 75 mm/s (Fig 1Go). The TRJ Doppler velocity was used to estimate RVSP by a modification of the Bernoulli formula: RVSP = RAPe + (peak TRJ velocity)2 x 4 [5]. Right atrial pressure (RAPe) was estimated at rest in the supine position by assessing the response of the inferior vena cava to normal and deep inspiration in the subcostal view (Fig 2Go). A RAPe of 3 mm Hg was recorded when the inferior vena caval diameter was small (<15 mm) and collapsed during spontaneous respiration. A RAPe of 7 mm Hg was recorded when the inferior vena caval diameter was of normal size (<20 mm) and it collapsed more than 50% with deep inspiration only. A RAPe of 17 mm Hg was recorded when the inferior vena caval diameter did not collapse more than 50% during deep inspiration [9]. All analyses were later made from videotape by one investigator (N.R.) blinded to type of operation, time after operation, and patient end points.



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  		Fig 1. . Transthoracic continuous-wave Doppler signal obtained from the tricuspid valve in a standard four-chamber view. The jet arising from tricuspid insufficiency has created the systolic signal whose peak velocity is 2.65 m/s.

 


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  		Fig 2. . (A) Inferior vena cava (IVC) during exhalation from the subcostal view. (B) The IVC compresses more than 50% during normal inspiration. (RT = right.)

 
Anesthetic and Postoperative Care
Patients received standard anesthetic management and continuous intraarterial monitoring, but invasive central venous pressure catheters were not routinely used. After operation, patients were monitored overnight in the postanesthesia care unit and returned to the thoracic surgical floor on the first postoperative day. Satisfactory postoperative analgesia was achieved in all patients either with continuous epidural fentanyl administration or with intravenous morphine patient-controlled analgesia. Surgical blood loss, intraoperative fluid intake and output, daily weights, and the use of theophylline or inhaled ß-agonist bronchodilators were recorded.

Statistical Analysis
Statistical analysis was performed with the SAS software version 6.04 (SAS Institute, Cary, NC). All variables were examined by two-tailed univariate analysis (Student's t test or Fisher's exact test). t Tests for estimated blood loss and intraoperative fluid management were computed after log transformation of data (due to nonnormal distribution). Repeated-measures analysis of variance was used for serial changes in echocardiographic parameters and in body weight. A p value less than 0.05 was considered significant. Data are presented as mean value ± standard deviation, unless otherwise indicated.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Eighty-six patients (mean age, 62 ± 10 years; range, 33 to 82 years) had major pulmonary resection. Patients undergoing lobectomy (n = 47) or pneumonectomy (n = 39) did not differ in age, sex, or preoperative medications (Table 1Go). Included in the pneumonectomy group were 10 patients who had an extrapleural pneumonectomy for mesothelioma. With the exception of a slightly lower preoperative carbon dioxide tension in the pneumonectomy group (p < 0.03), preoperative pulmonary function studies did not differ (see Table 1Go).


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  		Table 1. . Patient Characteristics
 
Echocardiography
In the lobectomy group, technically adequate echocardiographic studies for TRJ determinations were obtained in 79% of patients preoperatively, in 87% on postoperative day 1, and in 79% on postoperative days 2 through 6 (Table 2Go). In the pneumonectomy group adequate TRJ determinations were possible in 77% of patients preoperatively, in 59% on postoperative day 1, and 77% on postoperative days 2 through 6 (see Table 2Go). The frequencies of RAPe values of 3, 7, and 17 mm Hg in the lobectomy group were 83%, 15%, and 2% at baseline, 81%, 17%, and 2% on postoperative day 1, and 89%, 9%, and 2% on postoperative days 2 through 6, respectively. In the pneumonectomy group the corresponding values were 82%, 13%, and 5% at baseline, 85%, 13%, and 2% on postoperative day 1, and 82%, 10%, and 8% on postoperative days 2 through 6, respectively. These frequencies did not differ between the groups.


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  		Table 2. . Echocardiographic Findings
 
Results of preoperative echocardiography between the groups did not differ with respect to left or right atrial size, right atrial pressure, TRJ Doppler velocity, or estimated RVSP (see Table 2Go). The above measurements were within the normal limits in both groups. However, on postoperative days 2 through 6 patients who had a pneumonectomy had a significantly higher RVSP than the patients who had a lobectomy (see Table 2Go). In comparison with the standard pneumonectomy patients (n = 29), those who had an extrapleural pneumonectomy (n = 10) did not differ in any measured or derived echocardiographic parameter throughout the study. Left ventricular ejection fraction was more than 0.50 in all patients throughout the study. Right ventricular enlargement was seen by echocardiography in 5 of 39 pneumonectomy patients and in 2 of 47 lobectomy patients (p = 0.24). All patients had a significant increase in heart rate on postoperative day 3 when compared with their preoperative baseline values (p < 0.001); however, the heart rate values between the groups were not different (see Table 2Go). Preoperative RVSP determination in the entire population (67/86) of patients correlated inversely to FEV1 % pred values (r = -0.24; p < 0.05) but not separately within the lobectomy (37/42) or pneumonectomy (30/39) groups. In the subset of patients with an FEV1 % pred less than 60%, RVSP determination correlated inversely with FEV1 % pred values (r = -0.78; p < 0.04) in the pneumonectomy group (8/9) but not in the lobectomy group (7/10) and only approached significance (r = -0.52; p < 0.06) when these two subsets of patients (19/86) were combined.

Lung Resection and Other Outcomes
Pneumonectomy patients had significantly more intraoperative bleeding (1,154 ± 1,148 versus 387 ± 423 mL; p = 0.0005) and received a greater amount of fluid and blood (2,459 ± 1,875 versus 1,679 ± 1,043 mL; p = 0.01), respectively, than lobectomy patients. This difference is due to the number of patients undergoing an extrapleural pneumonectomy for mesothelioma within the entire pneumonectomy group (10/39). Mean blood loss was substantially greater (p < 0.0001) for extrapleural pneumonectomy patients (2,180 ± 1,063 mL) than for standard pneumonectomy (800 ± 959 mL) or lobectomy (387 ± 423 mL) patients. No difference was seen in the perioperative weight change or in hospital stay, 30-day morbidity, or mortality (Table 3Go) between the groups. The incidence of combined morbidity and mortality did not differ in the patients with an RVSP of 30 mm Hg or more (upper limit of normal) on postoperative days 2 through 6 between the two groups or in the entire population. In the 4 patients who died, preoperative echocardiography showed normal RVSP and no right atrial or ventricular enlargement. However, with progression of acute respiratory distress syndrome in 3 patients right ventricular enlargement worsened in 2 of these 3 patients.


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  		Table 3. . Operation and Outcome
 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Our study demonstrates that pneumonectomy leads to a modest increase in RVSP as estimated by the TRJ Doppler velocity method. We could not demonstrate, however, important increases in right atrial size or pressure from preoperative baseline values in either the pneumonectomy or lobectomy group. Similarly, the incidence of right ventricular enlargement by echocardiography was low in both groups and worsened in those patients in whom respiratory failure developed. Clinical [10] and experimental [11] reports suggest that the etiology for the early increase in right heart pressure after pneumonectomy is most likely due to the decrease in volume of the pulmonary vascular bed [10, 11] and to heightened activity of the adrenergic system early after operation [12]. In subjects with normal pulmonary vascular tone the cardiac output needs to increase by 2.5 times the normal value to produce any increase in the mean pulmonary artery pressure [10]. Comparable increases in cardiac output across the pulmonary vascular bed occur after pneumonectomy and with increased physical activity after a major pulmonary operation. Although we did not measure cardiac output, the increase in RVSP on postoperative days 2 through 6 but not on postoperative day 1 in our pneumonectomy group corresponds to the time of increased physical activity after operation. The relatively rigid or restricted pulmonary vasculature of patients with advanced COPD may not be able to accommodate even small increases in pulmonary blood flow. This is consistent with our observation that preoperative RVSP values were inversely correlated in the subset of patients with an FEV1 % pred less than 60% undergoing pneumonectomy. The inability to tolerate increases in blood flow may be an important contributing factor to the development of postpneumonectomy pulmonary hypertension [10].

The early [2–4] effects of lung resection on the pulmonary circulation have been reported in studies involving small numbers of nonambulating patients undergoing primarily lobectomy. These authors observed mild elevations in pulmonary vascular resistance and in right ventricular end-diastolic volume and decreased right ventricular ejection fraction [2] using pulmonary artery catheters 1 to 3 days after thoracic operation. In contrast to the above reports, we employed serial echocardiography in ambulating postoperative patients to assess cardiac function in near-physiologic conditions and did not find a significant incidence of right ventricular systolic dysfunction in either lobectomy or pneumonectomy patients despite the increase in right heart pressure seen in the latter group. The advantages of echocardiography when compared with right heart catheterization derived hemodynamic variables, however, include the noninvasive nature of ultrasound, which allows real-time assessment of right or left atrial and ventricular size as well as function. The obvious limitations of echocardiography are the need for technical support, cost, and its limitation as a bedside monitor. In critically ill patients after major pulmonary resection, in whom right heart catheterization may not be desirable, postoperative echocardiography combined with central venous pressure monitoring may be a reliable alternative to aid in their management. To investigate later alterations in right heart function, purported to occur after pneumonectomy, a long-term follow-up with echocardiography is warranted.

Several groups of investigators have attempted to identify patients at high risk for perioperative morbidity and mortality by incorporating either hemodynamic measurements or exercise testing of patients scheduled for major pulmonary resection [13–18]. Our data in an adequate sample size also failed to show any additional information provided by preoperative echocardiography in patients with varying degrees of COPD. The preoperative echocardiographic indices of right heart function in our entire patient population were within the normal range except in the subset of patients scheduled for pneumonectomy with an FEV1 % pred less than 60%. Due to the intricate relationship of the preoperative cardiovascular and pulmonary status of the patient and the effect of operation it is unlikely that a single preoperative or intraoperative variable of cardiac or pulmonary reserve will be predictive of poor postoperative outcome. Instead, an approach combining high-risk criteria such as preoperative chemotherapy use, poor performance on cardiac or pulmonary evaluation, and type of operation (pneumonectomy) may prove beneficial if validated in a large study.

In conclusion, an early postoperative increase in right heart pressure was more common after pneumonectomy than lobectomy but did not appear to adversely affect right ventricular systolic function. Our data support the current opinion that routine preoperative evaluation of right heart function is not justified in this patient population but suggest that perioperative echocardiography can be useful to evaluate cardiac function in patients in whom respiratory failure develops after lobectomy or pneumonectomy. The role of right heart afterload reduction in conjunction with respiratory support to prevent irreversible right ventricular enlargement in this subset of patients may warrant investigation in future trials.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Ilana Ginsburg, RN, for technical assistance; Manjit S. Bains, MD, Patricia M. McCormack, MD, and Valerie W. Rusch, MD, for their assistance; and Ms Barbara Viets for preparing the manuscript.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Amar, Department of Anesthesiology and Critical Care Medicine, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Mlczoch J, Zutter W, Keller R, Herzog H. Influence of lung resection on pulmonary circulation and lung function at rest and on exercise. Respiration 1975;32:424–35.[Medline]
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  3. Reed CE, Dorman BH, Spinale FG. Assessment of right ventricular contractile performance after pulmonary resection. Ann Thorac Surg 1993;56:426–32.[Abstract]
  4. Lindgren L, Lepantalo M, von Knorring J, Rosenberg P, Orko P, Scheinin B. Effect of verapamil on right ventricular pressure and atrial tachyarrhythmia after thoracotomy. Br J Anaesth 1991;66:205–11.[Abstract/Free Full Text]
  5. Himelman RB, Stulbarg M, Kircher B, et al. Noninvasive evaluation of pulmonary artery pressure during exercise by saline-enhanced Doppler echocardiography in chronic pulmonary disease. Circulation 1989;79:863–71.[Abstract/Free Full Text]
  6. Tamarin R, Torbicki A, Marchandise B, Laaban JP, Morpungo M. Doppler echocardiographic evaluation of pulmonary artery pressure in chronic obstructive pulmonary disease. A European multicentre study. Eur Heart J 1991;12: 103–11.[Free Full Text]
  7. Amar D, Roistacher R, Burt M, Reinsel RA, Ginsberg RJ, Wilson RS. Clinical and echocardiographic correlates of symptomatic tachydysrhythmias after noncardiac thoracic surgery. Chest 1995;108:349–54.[Medline]
  8. Morris JF, Koski A, Johnson LC. Spirometric standards for healthy nonsmoking adults. Am Rev Respir Dis 1971;103: 57–67.[Medline]
  9. Schiller NB. Pulmonary artery pressure estimation by Doppler and two-dimensional echocardiography. Cardiol Clin 1990;8:277–87.[Medline]
  10. Robin ED, Gaudio R. Cor pulmonale. Disease-A-Month 1970; May:1–38.
  11. Hsia CCW, Carlin JI, Cassidy SS, Ramanathan M, Johnson RL Jr. Hemodynamic changes after pneumonectomy in the exercising foxhound. J Appl Physiol 1990;69:51–7.[Abstract/Free Full Text]
  12. Smiley RM, Pantuck CB, Morelli JJ, Chadburn A, Knowles DM. Alterations of the ß-adrenergic receptor system after thoracic and abdominal surgery. Anesth Analg 1994;79:821–8.[Abstract/Free Full Text]
  13. Brundler H, Chen S, Perruchoud AP. Right heart catheterization in the pre-operative evaluation of patients with lung cancer. Respiration 1985;48:261–8.[Medline]
  14. Fee HJ, Holmes EC, Gewirtz HS, Ramming KP, Alexander JM. Role of pulmonary vascular resistance measurements in preoperative evaluation of candidates for pulmonary resection. J Thorac Cardiovasc Surg 1978;75:519–24.[Abstract]
  15. Laros CD, Swierenga J. Temporary unilateral pulmonary artery occlusion in the preoperative evaluation of patients with bronchial carcinoma. Med Thorac 1967;24:269–83.[Medline]
  16. Reilly JJ, Mentzer SJ, Sugarbaker DJ. Preoperative assessment of patients undergoing pulmonary resection. Chest 1993;103:342S–5S.[Medline]
  17. Olsen GN, Weiman DS, Bolton JWR, et al. Submaximal invasive exercise testing and quantitative lung scanning in the evaluation for tolerance of lung resection. Chest 1989;95:267–73.[Medline]
  18. Lewis JW 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;108:169–75.[Abstract/Free Full Text]



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