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Ann Thorac Surg 2007;83:1986-1992
© 2007 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Cardiac Function and Position More Than 5 Years After Pneumonectomy

Sietske A. Smulders, MDa, Sebastiaan Holverda, MSe, Anton Vonk-Noordegraaf, MD, PhDe,*, Harrie C.M. van den Bosch, MDb, Johannes C. Post, MD, PhDc, J. Tim Marcus, PhDd, Frank W.J.M. Smeenk, MD, PhDa, Pieter E. Postmus, MD, PhDe

a Department of Pulmonary Diseases, Catharina Hospital, Eindhoven, the Netherlands
b Department of Radiology, Catharina Hospital, Eindhoven, the Netherlands
c Department of Cardiology, Catharina Hospital, Eindhoven, the Netherlands
d Department of Physics and Medical Technology, VU University Medical Center, Amsterdam, the Netherlands
e Department of Pulmonary Diseases, VU University Medical Center, Amsterdam, the Netherlands

Accepted for publication January 22, 2007.

* Address correspondence to Dr Vonk-Noordegraaf, Department of Pulmonary Diseases, VU University Medical Center, PO Box 7057, Amsterdam 1007 MB, the Netherlands (Email: a.vonk{at}vumc.nl).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Pneumonectomy not only reduces the pulmonary vascular bed but also changes the position of the heart and large vessels, which may affect the function of the heart. We investigated long-term effects of pneumonectomy on right ventricular (RV) and left ventricular (LV) function and whether this function is influenced by the side of pneumonectomy or the migration of the heart to its new position.

Methods: In 15 patients who underwent pneumonectomy and survived for more than 5 years, we evaluated by dynamic magnetic resonance imaging the function of the RV and LV and the position of the heart within the thorax.

Results: Long-term effect of pneumonectomy on the position of the heart is characterized by a lateral shift after right-sided pneumonectomy and rotation of the heart after left-sided pneumonectomy. Postoperatively, heart rate was high (p = 0.006) and stroke volume was low (p = 0.001), compared with the reference values, indicating impaired cardiac function. Patients after right-sided pneumonectomy had an abnormal low RV end-diastolic volume of 99 ± 29 mL together with a normal LV function. No signs of RV hypertrophy were found. In left-sided pneumonectomy patients, RV volumes were normal whereas LV ejection fraction was abnormally low.

Conclusions: The long-term effects of pneumonectomy on the position of the heart are characterized by a lateral shift in patients after right-sided pneumonectomy and rotation of the heart in patients after left-sided pneumonectomy. Overall, cardiac function in long-term survivors after pneumonectomy is compromised, and might be explained by the altered position of the heart.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Major lung resection, especially pneumonectomy, decreases ventilatory function and has significant effects on right ventricular (RV) function [1–3]. Immediately after pneumonectomy, the RV dilates and RV ejection fraction decreases [4, 5]. Increasing RV afterload due to rising pulmonary artery pressure and pulmonary vascular resistance occurring after major lung resection is supposed to be the main cause of this RV dysfunction [4]. However, it is unclear to what extent the early postpneumonectomy RV dysfunction recovers in the long term and whether this may still play a role in the exercise limitation of postpneumonectomy patients.

Pneumonectomy not only changes the pulmonary hemodynamics but also leads to a migration of the heart and large vessels through the thoracic cavity, a process that takes years after the resection. Owing to the production of fibrotic tissue in the empty pleural space, intrathoracic pressure changes, with elevation of the diaphragm and overdistension of the remaining lung, the heart and mediastinum shift to the side that was operated on. These changes might induce alterations in cardiac structure and function, which might be different after left-sided pneumonectomy in comparison with right-sided pneumonectomy, and depending on the position of the heart in the thoracic cavity. However, this has not been studied until now, as the altered cardiac position hampers the use of echocardiography in these pneumonectomy patients. For this reason, we used cardiovascular magnetic resonance imaging (MRI) in this study because this technique has the advantage of being independent on the geometric assumptions and acoustic windows that limit echocardiography [6]. The aim of the present study was to measure the effects of right- and left-sided pneumonectomy on the structure and function of the heart, more than 5 years after the operation.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
We studied 15 consecutive patients presenting for a routine follow-up examination in an academic and in a nonuniversity teaching hospital. At that time, approximately 10 pneumonectomies were done in both hospitals each year. All patients studied underwent pneumonectomy more than 5 years ago. No signs of emphysema or interstitial lung disease were visible on the preoperative computed tomography scan. No other significant pulmonary or cardiac diseases were present before pneumonectomy, except lung cancer. None of the patients received chemotherapy or radiotherapy before surgery. Informed consent was obtained from all subjects, and the local Ethics Committees approved the study.

Lung Function and Cardiopulmonary Exercise Testing
We performed lung function (vital capacity and forced expiratory volume in 1 second [FEV1]) and maximal incremental exercise tests (maximum workload [Wmax], maximum oxygen uptake during exercise [VO2max], and ventilation at maximum exercise [VEmax]) in accordance with the American Association for Respiratory Care [7] and European Respiratory Society criteria [8] in all patients. Standard equipment Vmax 229 and 6200 (SensorMedics, Yorba Linda, California) for the academic center and standard equipment (Oxycon Beta and Masterlab; Viasys, Bilthoven, Netherlands) for the nonacademic center, were used for all pulmonary function tests. During maximal incremental exercise test, patients’ measurements were recorded after a 3-minute resting period on the bicycle, after which patients started exercising at a constant speed of 60 rpm at 0W for 2 minutes. A ramp protocol based on patient’s age, sex, and FEV1 followed until patients were exhausted. Recovery period lasted 6 minutes. The Vslope method was used to determine whether the anaerobic threshold was reached [9].

Geometric Position of the Heart
Using the four-chamber view images according to the method depicted in Figure 1, we established the degree of rotation of the heart in each patient. In normal patients, the angle of the interventricular septum with the anteroposterior line (through the middle of the sternum and the middle of the spinal cord) is approximately 70 degrees. This angle was used as the reference angle, and set at 0 degrees. Clockwise rotation resulted in a negative angle and counterclockwise rotation in a positive angle (Fig 1). By doing this, we tried to establish any difference in degree of rotation of the hearts in our patients.


Figure 1
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  		Fig 1. Assessment of the degree of rotation of the heart, by measuring the angle (*) between a normally positioned interventricular septum (set at 0 degrees) and the position of the interventricular septum in the postpneumonectomy heart. Clockwise rotation results in a negative angle and counterclockwise rotation in a positive angle. (A = apex of left ventricle; LV = left ventricle; RV = right ventricle.)

 
Magnetic Resonance Imaging Protocol
The patients were scanned [10] using a 1.5 T Siemens Sonata whole body system (Siemens Medical Systems, Erlangen, Germany) in the academic center, or the 1.5 T Philips Intera, software release 10.3 (Philips Medical Systems, Best, Netherlands) in the nonacademic teaching center. On both systems, a phased-array body coil was applied. All image acquisition was prospectively triggered by the R-wave of the electrocardiogram. The subject was instructed to hold his or her breath in moderate inspiration during all image acquisitions.

Short-axis ventricular imaging
The horizontal long-axis view was determined in a late diastolic frame using a black-blood prepared turbo gradient-echo sequence [10]. Then a breath-hold cine acquisition was performed of this long-axis view. By using the end-diastolic cine frame of this long-axis view, a series of parallel short-axis image planes was defined starting at the base of the left ventricle (LV) and RV, and encompassing the entire LV and RV from base to apex. The most basal image plane was positioned close to the transition of the myocardium to the mitral and tricuspid valve leaflets (at a distance of half the slice thickness). This ensured that also the most basal part of the LV and RV was covered. At every short-axis plane, a breath-hold cine acquisition was then performed (temporal resolution <40 ms). Slice thickness was 6 mm and gap, 4 mm. Thus, the slice distance was 10 mm. Heart rate was monitored during the acquisition of the short-axis images.

Image analysis
The images were processed on a Sun Sparc station using the MASS software package (Department of Radiology, Leiden University Medical Center, Leiden, Netherlands) for the Siemens scanner and on a View Forum (release 3.2) workstation with a dedicated cardiac analysis software package for the Philips. End-diastole was defined as the first temporal frame directly after the R-wave of the electrocardiogram. End-systole was defined as the temporal frame at which the image showed the smallest right and left ventricular cavity area, usually 240 to 320 ms after the R-wave. Epicardial and endocardial contours were manually traced, and the papillary muscles were excluded from the RV and LV volume and included with the RV and LV mass as described before [10]. The LV end-diastolic mass was obtained from the volume of the LV muscle tissue including the interventricular septum, the RV end-diastolic mass in a similar way, but excluding the septum. In the mass calculation, the specific weight of muscle tissue was 1.05 g/cm3.

Data Analysis
Results on lung function, exercise tests, and cardiac function were compared between patients after left- and right-sided pneumonectomy. Results on RV and LV function in pneumonectomy patients were compared with normal ventricular dimensions for MRI from healthy controls (n = 25). Recently, data from these healthy controls were in part also presented by Vonk-Noordegraaf and associates [11]. This is one of the few recent studies on establishment of these values, addressing both LV and RV structure and function in adults. Other studies that obtained reference values for LV [10, 12, 13] and RV [12, 13] function by MRI provided only information on the LV (Marcus and associates [10]) or included children (Lorenz and coworkers [12]) in their study group.

Statistical Analysis
We used SPSS 13.0 (SPSS, Chicago, Illinois) for statistical analysis. Mann-Whitney U tests for independent samples were used to determine differences comparing healthy controls with patients and comparing patients after left- or right-sided pneumonectomy regarding cardiac function, lung function, and exercise tolerance. Statistical significance was set at p less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Mean age of all patients was 64.3 years (range, 47 to 80), and mean time after pneumonectomy 106.5 months (range, 62 to 191). Mean age of the healthy controls was significantly lower compared with our patients (Table 1). Preoperatively, mean FEV1 percent of predicted, mean Wmax percent of predicted, and mean VO2max percent of predicted were 84.6 ± 14.1, 101.4 ± 42.3, and 86.5 ± 30.4, respectively. In 1 patient, the phrenic nerve was crushed during left-sided pneumonectomy with the surgeons’ intention to enhance filling of the postpneumonectomy space. Postoperatively, chest tubes were placed in all patients and connected to a balanced drainage system during the first short postoperative period. The postoperative course in 1 patient who underwent pneumonectomy with partial resection of the pericardium was complicated by the development of insufficiency of the tricuspid valve, and in another patient by the development of residual cancer on the bronchial stump for which he underwent a curative re-resection, complicated by hypertension and viral pericarditis, which were treated. One patient received medication (nifedipine) for the treatment of systemic hypertension.


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  		Table 1 Postoperative LV and RV Function a Comparing Patients With Healthy Controls and Comparing Patients After Right- and Left-Sided Pneumonectomy
 
Lung Function and Cardiopulmonary Exercise Testing
Lung function and exercise tests were done more than 5 years after pneumonectomy in all patients except 1, who underwent the exercise test at 28 months after surgery. We found no statistically significant differences regarding lung function or exercise capacity comparing patients after right- or left-sided pneumonectomy. Mean percent of predicted forced vital capacity and FEV1 were 58.2 ± 14.3) and 49.1 ± 10.6, respectively. All patients reached their anaerobic threshold during the exercise test. Mean VO2max, Wmax, and VEmax were 15.1 mL · min–1 · kg–1 (± 3.3), 84.1 watt (± 33.3), and 41.6 L/min (± 12.7), respectively, which were 62%, 56%, and 77% of predicted. Mean oxygen pulse at maximum exercise was 9.7 ± 3.1 mL/beat, with markedly impaired progression from rest to maximum exercise of 219% ± 76%. Patients after left-sided pneumonectomy tended to have lower VO2max % of predicted (56.5 ± 11.9) compared with right-sided pneumonectomy patients (70.6 ± 16.5), although this was not significant.

MRI Measurements
Magnetic resonance imaging scans were performed in all patients, with a mean time interval between the pneumonectomy and the MRI of 101 months (range, 60 to 179) postoperatively. Reviewing MRI scan results revealed a myocardial infarction in 1 patient, which has not been diagnosed previously (Fig 2II).


Figure 2
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  		Fig 2. Four-chamber views of all patients after left-sided pneumonectomy. Below each separate figure, the angle of rotation is presented. Anatomical orientation of the separate figures is as follows: top = ventral; bottom = dorsal; right = left side of patient; left = right side of patient. (Star = left ventricular cavity; rhombus = right ventricular cavity.)

 
Geometric Measurements
Figure 2 (for left-sided pneumonectomy patients) and Figure 3 (for right-sided pneumonectomy patients) present an overview of four-chamber views by MRI of all patients who were studied. All patients demonstrated some degree of mediastinal shift, which seemed to be more extensively in case the postpneumonectomy space was completely obliterated (Figs 2IV, V, VIII, and 3III). Using the method depicted in Figure 1, we established the degree of rotation of the hearts in our patients. We found that after left- and right-sided pneumonectomy respectively, the mean degree of rotation was 28 ± 62 degrees (range, 96 to 102) and 33 ± 9 degrees (range, 23 to 44). Resulting from this and from Figures 2 and 3, it is clear that after left-sided pneumonectomy, the heart and vascular structures not only shift into the left hemithorax but also rotate, while the extent of rotation extremely varied between patients. In contrast, rotation of the heart was nearly absent after right-sided pneumonectomy, and mostly signs of lateral shifting of the heart and vessels were found in these patients. No correlation was found between the degree of rotation and the LV and RV end-diastolic volumes or LV ejection fraction.


Figure 3
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  		Fig 3. Four-chamber views of all patients after right-sided pneumonectomy. Below each separate figure, the angle of rotation is presented. Anatomical orientation of the separate figures is as follows: top = ventral, bottom = dorsal, right = left side of patient, left = right side of patient. (Star = left ventricular cavity; rhombus = right ventricular cavity.)

 
Cardiac Function
In Table 1, results on RV and LV function are presented, comparing patients with healthy controls and comparing patients after left- and right-sided pneumonectomy. Although cardiac output was normal in all patients, stroke volume was significantly lower (p = 0.001), compensated by an increased resting heart rate (p = 0.006) compared with healthy controls. No significant difference in stroke volume was observed between the right- and left-sided pneumonectomy patients.

Patients after left-sided pneumonectomy had an increased LV end-diastolic volume together with a decrease in LV ejection fraction, whereas RV volumes were normal. In contrast, patients after right-sided pneumonectomy had signs of RV hypotrophy together with a decreased RV end-diastolic volume (99 ± 29 mL), while LV volume and function were normal.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Our study shows that in a group of long-term survivors after pneumonectomy (more than 5 years), considerable intrathoracic anatomical changes occur together with a reduction of stroke volume compensated by an increased heart rate at rest, indicative of compromised cardiac function. Although we did not measure stroke volume during exercise, the abnormal stroke volume response during exercise in the presence of a normal ventilatory reserve at maximal exercise provides further evidence that cardiovascular limitation contributes to the limited exercise capacity in these patients. As we did not find any signs of RV hypertrophy, the decreased stroke volume is unlikely due to increased pulmonary artery pressures (increased afterload). Furthermore, we conclude that based on the differences found between right- and left-sided pneumonectomy patients, the RV underfilling is the primary factor that compromised RV function, whereas LV failure is the primary factor in left-sided pneumonectomy patients. Overall, however, we would like to point out that, considering their specific situation, cardiac function in these long-term survivors was relatively well preserved.

Previous studies by Biondetti and colleagues [14] and Suarez and associates [15] have mentioned the finding of more extreme mediastinal shifting in case the postpneumonectomy space is completely obliterated. Although we did not relate the amount of pleural filling with the lung function, it is clear from the MRI images that there is variation in the amount and location of pleural filling and both hemidiaphragms influencing the expansion of the remaining lung. None of our patients showed evidence for left-sided pneumonectomy syndrome or compression of the left main bronchus after right-sided pneumonectomy [16, 17].

Our findings show that mostly rotation of the heart occurs after left-sided pneumonectomy and that there is a huge variability between patients. Factors that determine the extent of rotation are unclear; however, it is conceivable that variation in the shape of the thoracic cavity, extent of elevation of the ipsilateral hemidiaphragm and degree of obliteration of the pleural cavity all might influence the final position of the heart. In contrast to this, the alteration of the heart in right-sided pneumonectomy patients is characterized by a lateral shift with only minor rotation of the heart. The extent of the lateral shift seemed to be determined by the degree of obliteration of the pleural space.

Although the group of patients was too small to draw firm conclusions on the effects of right-sided pneumonectomy in comparison with left-sided pneumonectomy on cardiac function, remarkable differences were observed between both groups. First, RV end-diastolic volume and LV mass were extremely low in patients after right-sided pneumonectomy. An explanation for this could be the lateral shift observed in these patients that possibly impairs RV filling owing to external compression of the thoracic wall. That could also explain the remarkably low RV mass we found after right-sided pneumonectomy. Low LV mass could be due to the effect of a chronically reduced stroke volume on the LV wall. Secondly, despite large standard deviations, patients after left-sided pneumonectomy seemed to have a relatively low LV ejection fraction and a significantly increased LV end-diastolic volume, compared with patients after right-sided pneumonectomy. Although we could not find a relation between LV ejection fraction and the degree of rotation of the heart, that does not preclude a causal relationship between cardiac rotation and loss of systolic function. However, the numbers were too small to perform further analysis. Although we cannot exclude a bias because our healthy controls were of significantly younger age compared with the pneumonectomy patients, age alone has little effect on cardiac structure and function [12].

We did not find any signs of RV hypertrophy or RV dilatation in our cohort, making the presence of pulmonary hypertension in our study population very unlikely. In the past few decades, several studies have reported on the effect of pneumonectomy on cardiopulmonary function (measurements ranging from 2 to 168 months postoperatively). In general, these studies agree that, in pneumonectomy patients, pulmonary artery pressure, RV systolic pressure, and pulmonary vascular resistance are normal or slightly increased at rest [18–24], and increase during exercise owing to the limited recruitment capacity of the pulmonary vascular bed, confirming our findings [1, 4, 19, 20]. That we did not find any signs of RV hypertrophy in our study could indicate that even in patients with some pulmonary hypertension, a not-to-large reduction of the pulmonary vascular bed (segmentectomy or even lobectomy) might be safe, because recently it was shown that RV hypertrophy is an early sign of adaptation of the RV to the intermittent pressure overload in chronic obstructive pulmonary disease patients [1]. Furthermore, Burrows and coworkers [19] found that RV hypertrophy only occurred in patients with an abnormal remaining lung. Because our patients had no signs of emphysema radiologically, we conclude that the pulmonary vascular bed in the remaining lung was sufficient to prevent the development of increased RV afterload.

In conclusion, this study shows that the long-term effects of pneumonectomy on the position of the heart are characterized by a lateral shift after right-sided pneumonectomy, whereas left-sided pneumonectomy leads to a rotation of the heart. Overall, cardiac function in long-term survivors after pneumonectomy is compromised, which might be explained by the altered position of the heart.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
Financial support for this manuscript was provided by Catharina Hospitals’ Scientific Fund and by GlaxoSmithKline Beecham, the Netherlands.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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