Ann Thorac Surg 1995;59:717-722
© 1995 The Society of Thoracic Surgeons
Transesophageal Echocardiography to Evaluate Patients With Severe Pulmonary Hypertension for Lung Transplantation
John Gorcsan, III, MD,
Todd D. Edwards, MD,
Galal M. Ziady, MD,
William E. Katz, MD,
Bartley P. Griffith, MD
Divisions of Cardiology and Cardiothoracic Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Accepted for publication December 6, 1994.
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Abstract
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The surgical approach to lung transplantation for patients with severe pulmonary hypertension will be dependent on the primary disease and specific cardiac anatomy. To determine the safety and utility of transesophageal echocardiography in the management of patients with severe pulmonary hypertension who are being evaluated for lung transplantation, we studied 48 consecutive patients, aged 38 ± 11 years, with pulmonary artery systolic pressure of 70 mm Hg or greater. All patients previously underwent left and right heart catheterization, transthoracic echocardiography, and radionuclide ventriculography. Transesophageal echocardiography was tolerated well by all patients. Additional data that significantly altered surgical therapy were found in 12 of 48 patients (25%): proximal pulmonary artery thrombi (3), patent foramen ovale with significant right to left shunting (2), atrial septal defect (2), double-outlet right ventricle (2), ventricular septal defect (2), and exclusion of atrial septal defect (1). These findings were confirmed surgically in all patients except 3, who died awaiting transplantation. Transesophageal echocardiography is useful in the evaluation of patients with severe pulmonary hypertension.
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Introduction
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Lung transplantation is a viable therapy for patients with severe symptomatic pulmonary hypertension and is being performed with increasing frequency [1–7]. The clinical presentation of adults with advanced pulmonary hypertension may be similar despite differing causes, such as Eisenmenger's physiology from a variety of congenital malformations, chronic thromboembolic disease, or primary pulmonary hypertension [8, 9]. The surgical therapy also may be markedly different for these diseases [1–7, 10–13]. An accurate diagnostic evaluation therefore is required of patients with severe pulmonary hypertension who are being considered as candidates for lung transplantation. Transesophageal echocardiography (TEE) provides high-resolution images that are superior to the transthoracic approach for detection of abnormalities of the base of the heart and proximal great vessels [14–19]. This additional information may affect the management of patients to include lung transplantation with cardiac repair versus lung transplantation alone, or heart-lung transplantation. Furthermore, the type of cardiac repair may be altered by this diagnostic information.
Before this study, a 39-year-old man underwent single-lung transplantation at our institution with the preoperative diagnosis of primary pulmonary hypertension. Preoperative transthoracic two-dimensional, spectral, and color Doppler echocardiograms were technically limited and did not reveal any intracardiac shunting. In addition, this patient had two right heart catheterizations at different institutions with oximetric studies that failed to diagnose any significant intracardiac shunt. Unfortunately, this patient died postoperatively of severe irreversible hypoxemia and pulmonary edema of the transplanted lung resulting from left to right shunting through a large secundum atrial septal defect (ASD), which was finally discovered by autopsy. Accordingly, this prospective study was undertaken to determine the safety and utility of TEE in providing new information that may alter the management of patients with severe pulmonary hypertension.
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Material and Methods
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Forty-eight consecutive adult patients with severe pulmonary hypertension, defined as pulmonary artery systolic pressures of 70 mm Hg or greater, referred to the University of Pittsburgh Medical Center from August 1991 to June 1992 for consideration for lung transplantation were studied prospectively. All patients gave written informed consent before study. There were 30 women and 18 men, aged 38 ± 11 years (range, 20 to 57 years).
All patients previously underwent diagnostic cardiac catheterization including oximetric right heart shunt studies, radionuclide ventriculography, ventilation/perfusion radionuclide lung scans, and transthoracic two-dimensional, spectral Doppler, and color Doppler echocardiography before TEE. Cardiovascular angiography, however, was limited to left ventriculography and coronary angiography in the majority of patients. The group mean pulmonary artery systolic pressure by catheterization was 101 ± 17 mm Hg (range, 70 to 135 mm Hg) with a group mean pulmonary artery mean pressure of 65 ± 11 mm Hg (range, 40 to 98 mm Hg). In addition, an extensive review of all medical records was performed to determine the initial diagnoses and all other known anatomic information before TEE. The diagnoses were as follows:
A 48-element biplane TEE transducer and ultrasound system were used (Hewlett-Packard Co, Medical Products Group, Andover, MA). All patients had continuous electrocardiographic, noninvasive blood pressure, and pulse oximetry monitoring. Patients with baseline pulse oximetry values of 90% or less were given supplemental oxygen. All studies were performed with 20% benzocaine oropharyngeal spray and intravenous sedation with midazolam (mean total dose, 4 ± 2 mg), supplemented with intravenous fentanyl (mean total dose, 79 ± 25 µg) in 12 patients. Complete two-dimensional, color, and spectral Doppler TEE examinations were recorded. Microbubble contrast studies were performed in all patients with injections of 10-mL increments of hand-agitated saline solution through a peripheral intravenous line. Any complication, including respiratory difficulties, persistent hypotension, cardiac arrhythmias, or bleeding was recorded.
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Results
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Transesophageal echocardiography was tolerated well by all patients without any complications. This included 9 patients with baseline oximetry values of less than 80% O2 saturation on room air.
Transesophageal echocardiography confirmed previous findings in 39 of 48 of patients studied and provided new information that significantly altered assignment of therapy in 12 patients or 25% (Table 1
). These 12 represented 33% of the patients with prior diagnoses of primary pulmonary hypertension or Eisenmenger's physiology.
Proximal pulmonary artery masses consistent with thrombi were found in 2 patients with pulmonary hypertension of uncertain cause (Fig 1) [19]. Both of these patients subsequently had diagnostic pulmonary angiography and underwent successful surgical thromboendarterectomy, rather than lung transplantation. Laminated mural thrombi within the pulmonary arteries were confirmed at the time of operation. Pulmonary artery masses suggestive of thrombosis were found in a third patient with a large ventricular septal defect (VSD). Based on these findings, single-lung transplatation was not considered as an option, and this patient underwent double-lung transplantation and VSD repair. In situ pulmonary artery thrombi were confirmed pathologically from the explanted lungs.
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Fig 1. . Images of a patient with pulmonary hypertension of uncertain cause before transesophageal echocardiography. Panel A shows a dilated and hypertrophied right ventricle (RV) and dilated right atrium (RA). Panel B shows a echodense mural mass within the right main pulmonary artery (RPA), which was surgically confirmed to be thrombus. (Ao = aorta; LA = left atrium; LV = left ventricle.)
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An unsuspected membranous VSD was found in a patient with a known large patent ductus arteriosus. A previous oximetric shunt study failed to diagnose this VSD likely because of systemic right ventricular pressures. In addition, poor-quality transthoracic echocardiographic studies failed to detect the VSD. The VSD was confirmed and closed at the time of double-lung transplantation and ductus arteriosus closure.
A secundum ASD was found in a patient previously thought to have severe pulmonary hypertension secondary to a VSD. Transesophageal echocardiography revealed a small muscular VSD, 3 mm in diameter, and a much larger (20 mm diameter) secundum ASD. These findings, which were confirmed surgically, changed the focus of the cardiac repair because it was highly unlikely that the small VSD was a significant contributor to the Eisenmenger's physiology.
Another patient who was thought previously to have a sinus venosus ASD and possible anomalous pulmonary venous drainage had an atrial septal aneurysm and ASD with normal pulmonary venous drainage demonstrated by TEE. These surgically confirmed findings altered the atrial cannulation site at the time of double-lung transplantation and ASD closure.
Another patient was originally diagnosed to have Eisenmenger's physiology from an ASD. This was based on a 7% oxygen step-up within the right atrium and a calculated 1.2 to 1 pulmonary to systemic flow ratio, along with a poor-quality transthoracic echo that suggested atrial septal dropout. An ASD was excluded by TEE imaging, color Doppler, and microbubble contrast injection with cough and Valsalva maneuvers. This patient's diagnosis was changed to primary pulmonary hypertension, and lung transplantation alone without median sternotomy or atriotomy was planned. Unfortunately, he died awaiting lung transplantation.
Abnormalities of the Ventricular Septum
Of the 12 patients with an original diagnosis of VSD, the ability for repair was unclear based on the anatomic information obtained by transthoracic echocardiography and contrast ventriculography in 5 patients [20]. Two patients were found to have a double-outlet right ventricle by TEE who were originally suspected to have uncomplicated VSDs (Fig 2). The surgical correction of a double-outlet right ventricle that would accompany lung transplantation would be more extensive and complex than a simple VSD closure, and these patients were listed for heart-lung transplantation [10, 11, 20]. In 3 patients, transthoracic imaging failed to demonstrate adequately ventricular septal and atrioventricular valve anatomy. Transesophageal echocardiography also was useful in evaluating the integrity of the mitral valve apparatus, which was helpful in selecting patients for heart-lung transplantation versus lung transplantation with VSD repair [11, 12, 20]. Two of these 3 patients had favorable anatomy for VSD repair with lung transplantation, and the remaining patient with a very large VSD has been listed for heart-lung transplantation (Fig 3).
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Fig 2. . Images of a patient thought to have a simple membranous ventricular septal defect before transesophageal echocardiography. Image A from the transgastric window with extreme anteflexion shows the aorta (Ao) arising from a dilated and hypertrophied right ventricle (RV), and a membranous ventricular septal defect (VSD). The pulmonary artery (PA) also was identified to arise from the RV. Images A and C show the aortic valve (AV) and pulmonic valve (PV) to be in the same plane and the ascending Ao and PA to be parallel. These findings were diagnostic of a double-outlet RV. (LA = left atrium; LV = left ventricle.)
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Fig 3. . Transesophageal echocardiographic images of a patient thought to have a simple membranous ventricular septal defect before transesophageal echocardiography. Image A is the midesophageal four-chamber view and image B is the transgastric short-axis view, which demonstrates a very large ventricular septal defect that was not suitable for surgical repair.
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Patent Foramen Ovale
Interatrial right to left shunting of microbubble contrast, specifically at the level of the fossa ovalis, was considered evidence of a patent foramen ovale (PFO) and was identified in 12 of the 41 patients (29%) with an otherwise intact atrial septum [21]. Contrast injections were accompanied by attempted cough and Valsalva maneuvers to maximize sensitivity of PFO detection, although approximately 30% of these sedated patients were unable to cooperate fully with these maneuvers. In 3 other patients, microbubble contrast was identified in the left atrium arising from the pulmonary veins, and thus was consistent with intrapulmonary shunting and not with a PFO. In 8 patients, only a trivial amount of shunting through a PFO was identified (arbitrarily defined as less than 10 bubbles). In 4 patients with a PFO, a larger amount of shunting was identified as more than 10 bubbles (Fig 4). Surgical therapy was altered to include PFO closure in these patients, and surgical conformation was accomplished. Of note, one patient with primary pulmonary hypertension underwent PFO closure from a right thoracotomy during lung transplantation, obviating the need for a median sternotomy. In the 8 patients with trivial shunting across a PFO, surgical closure was not performed routinely during lung transplantation. Although long term follow-up data are unavailable, the immediate postoperative outcome did not appear to be affected unfavorably by not closing the small PFO in these patients. Accordingly, the finding of a PFO with trivial shunting by TEE in patients with very high right heart pressures was not considered a significant finding that would alter therapy in this study.
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Fig 4. . Transesophageal echocardiographic images of a patient with a patent foramen ovale (A) and right-to-left shunting demonstrated by microbubble contrast injection (B). (LA = left atrium; RA = right atrium.)
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Comment
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Transesophageal echocardiography can provide high-resolution images of cardiovascular anatomy and has been shown to be superior to transthoracic echocardiography in diagnosing congenital heart disease in adults [14–19]. This study extends the diagnostic utility of TEE to patients with severe pulmonary hypertension by providing new diagnoses that significantly altered management in 25% of this series of patients, including 33% with the prior diagnoses of primary pulmonary hypertension or Eisenmenger's physiology. This new information was not obtained by previous invasive and noninvasive studies.
Accurate anatomic information is of particular importance in patients being evaluated for lung transplantation for several reasons. The immediate success of lung transplantation may be dependent on the ability to correct concomitant congenital heart defects at the time of transplantation. Single- and double-lung transplantation now are performed using unilateral or bilateral thoracotomies, rather than a median sternotomy approach. Accordingly, intraoperative diagnoses by direct surgical inspection of the cardiac anatomy cannot be accomplished. The reduction of right heart pressures from lung transplantation without the correction of an intracardiac shunt defect may result in severe left to right shunting in the immediate postoperative period, which would further augment the high flow to the transplanted lung and may result in acute pulmonary edema and allograft failure [7]. It also is important to assign patients correctly in whom surgical correction of complex congenital defects would not be possible to heart-lung transplantation rather than lung transplantation [11, 12, 20].
Transesophageal echocardiography has demonstrated utility as an adjunctive procedure to a conventional invasive and noninvasive evaluation of patients with severe pulmonary hypertension for the following reasons. First, the clinical presentation of adults with severe pulmonary hypertension from Eisenmenger's pulmonary vascular disease that has resulted from unsuspected congenital anomalies may be similar to other forms of pulmonary hypertension, such as chronic thromboembolic disease or primary pulmonary hypertension [8, 9]. Second, patients with Eisenmenger's physiology who first are evaluated after the development of markedly elevated right heart pressures may have bidirectional shunting, which may interfere with the accuracy of oximetric catheterization studies [22]. Third, extensive invasive angiographic studies that would involve right ventricular and pulmonary artery contrast injections may be tolerated poorly by patients with severe pulmonary hypertension, and this increased risk does not favor the invasive diagnostic approach [23, 24]. Transesophageal echocardiography, including sedation and microbubble contrast injections, was well tolerated by all patients in this study, although close monitoring and avoidance of excessive sedation must be emphasized in these patients. Fourth, TEE, when compared with the transthoracic approach in the same patients, has demonstrated superior ability to diagnose correctly cardiovascular abnormalities, in particular of the interatrial and ventricular septa, pulmonary veins, and proximal aorta and pulmonary arteries [14–19].
Of the group of 12 patients in whom TEE provided new information that altered assignment of surgical therapy, 3 patients died while awaiting lung transplantation, and autopsy data were not available in these patients. However, surgical confirmation of TEE data that influenced surgical therapy was obtained in all of the remaining patients.
Another potential limitation of this study is that peripheral injections of microbubble contrast to detect intracardiac shunting were performed only during transthoracic echocardiography in approximately 50% of patients. Although recent data support transthoracic imaging for detecting small shunts such as PFO, especially with lower extremity microbubble injections [25], it often is difficult to differentiate intrapulmonary shunting from intracardiac shunting without high-resolution imaging of the fossae ovalis and pulmonary veins. In addition, more detailed information of atrial septal anatomy is needed to dictate surgical closure rather than detection of interatrial shunting alone [15].
A final potential limitation of this study is that few patients had angiographic imaging of more than their left ventricles and coronary arteries, and it is possible that correct diagnoses would be obtained with more extensive angiographic evaluations. However, radiocontrast injections into the right ventricles or pulmonary arteries may not be tolerated well by patients with severe pulmonary hypertension, and they are at increased risk for complications [23, 24]. Transesophageal echocardiography does not require radiocontrast injections, and is well tolerated as suggested by our initial experience reported here.
In conclusion, TEE provides additional information that may alter assignment of surgical therapy in a significant portion of patients with severe pulmonary hypertension who are being evaluated for lung transplantation. It is particularly useful in patients who are suspected to have either primary pulmonary hypertension or Eisenmenger's physiology. Transesophageal echocardiography appears safe and well tolerated in this group of severely ill patients, and should be considered as a useful adjunct in the evaluation of patients for lung transplantation.
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Acknowledgments
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We thank Jose Ettedgui, MD, for careful review of the manuscript and his valuable suggestions. We are grateful for the contributions of Daniel Foust, RN, Jan Manzetti, RN, and the entire lung transplantation team. We also thank Christie Bennett for administrative assistance and preparation of the manuscript.
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Footnotes
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Address reprint requests to Dr Gorcsan, Division of Cardiology, University of Pittsburgh Medical Center, 3550 Terrace, Scaife Hall, Rm 548, Pittsburgh, PA 15261.
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Abstract
Introduction
