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Ann Thorac Surg 1999;67:146-152
© 1999 The Society of Thoracic Surgeons


Original Articles

Use of transesophageal echocardiography for postoperative evaluation of right ventricular function

Yoshie Ochiai, MDa, Shigeki Morita, MDa, Yoshihisa Tanoue, MDa, Yoshito Kawachi, MDa, Ryuji Tominaga, MDa, Hisataka Yasui, MDa

a Department of Cardiovascular Surgery, Faculty of Medicine, Kyushu University, Fukoka, Japan

Accepted for publication July 14, 1998.

Address reprint requests to Dr. Morita, Department of Cardiovascular Surgery, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
e-mail: morita{at}heart.med.kyushu-u.ac.jp


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. No method has been available to assess the right ventricular (RV) pressure–volume relation in the operating room or intensive care unit. Left ventricular cross-sectional area measured by echocardiography using the technology of automated border detection has been used to construct left ventricular pressure–area (P-A) loops. In the human right ventricle, however, this approach has not been validated.

Methods. We recorded RV P-A loops in 14 patients in the intensive care unit using transesophageal echocardiography. Multiple RV P-A loops were obtained by reducing preload with intravenous nitroglycerin, thereby elucidating the end-systolic P-A relation.

Results. With an incremental dose of dobutamine, the slope of the RV end-systolic P-A relation increased (from 4.56 ± 2.42 to 7.34 ± 3.62 mm Hg/cm2, p < 0.01), with no change in the x-axis intercept, which implied increased contractility. Furthermore, in the operating room we validated the use of RV cross-sectional area as a surrogate for RV volume by demonstrating the close correlation between the stroke area (maximal RV area minus minimal RV area) and stroke volume (r = 0.962; p < 0.0001).

Conclusions. Tranesophageal echocardiography with automated border detection is a promising tool for elucidating RV function through the analysis of RV P-A loops.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The importance of understanding right ventricular (RV) performance has become evident recently, especially in patients with severe left heart failure [1] and left ventricular (LV) assist device implantation [2]. For evaluation of load-independent ventricular function variables, assessment of the end-systolic pressure–volume relation (ESPVR) is required. Right ventricular chamber volume, however, is technically difficult to determine because of its complex anatomic geometry. Instantaneous measurement of RV volume may be possible by use of a three-dimensional echocardiographic method [3] or cine magnetic resonance imaging [4], but these approaches are impractical in the operating room or intensive care unit.

Echocardiographic automated border detection (ABD) is a new technique that is capable of continuously measuring ventricular cavity area by differentiating the acoustic backscatter characteristics of blood from myocardial tissue [5]. Using ABD technology, instantaneous measurement of the cross-sectional area (CSA) is possible. The pressure–area (P-A) relations obtained with ABD capabilities were previously reported to assess LV contractility in both animal and human studies, with LV cavity area as a surrogate for volumes [69]. However, few studies have applied this technology to assess RV contractility. Accordingly, the present study was undertaken to determine (1) whether on-line measurement of RV CSA could accurately estimate changes in stroke volume (SV) by comparing simultaneously recorded RV CSA with instantaneous pulmonary blood flow in the operating room; (2) whether the technique of ABD could define the RV end-systolic P-A relation (ESPAR) in the clinical setting; and (3) whether the obtained RV ESPAR could reflect the changes in the contractile state. The results indicate that on-line measurement of RV P-A loops with transesophageal echocardiography (TEE) is a potentially promising method for elucidating RV contractility in patients undergoing open-heart surgical procedures.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Validation study in the operating room
A total of 9 patients undergoing open-heart surgical intervention (atrial septal defect closure in 3, mitral valve repair for mitral regurgitation in 6) were studied in the operating room. The study protocol was approved by the human investigation committee of our institution. Written informed consent was obtained from each patient. Patients were placed in a supine position. After the induction of anesthesia we positioned a rapid-response thermistor pulmonary artery catheter (7.5F Swan-Ganz catheter, model 93A-431H; Baxter Healthcare Corp, Irvine, CA) in the pulmonary artery and a catheter-tipped micromanometer (Sentron; AC Roden, the Netherlands) in the right ventricle just under the pulmonary valve. These two catheters were inserted percutaneously, and the position of the catheters was verified on chest X-ray film.

A 5-MHz omniplane transesophageal echocardioscope (model HP 21362C; Hewlett-Packard, Andover, MA) was inserted. Immediately after cardiopulmonary bypass, an electromagnetic flow probe (model FR series; Nihon Koden, Tokyo, Japan) was positioned around the main pulmonary artery to measure volumetric pulmonary artery flow by a flow meter (MFV-2100; Nihon Koden). A plastic water-filled pressure line was inserted into the left atrium from the right upper pulmonary vein to measure left atrial pressure.

Protocol
The study was performed immediately after the patients were taken off cardiopulmonary bypass. The recordings of the RV CSA and pulmonary artery flow wave were evaluated for quality. When satisfactory images and flow wave recordings were confirmed, the respirator was transiently disconnected from the endotracheal tube. The inferior vena cava was slowly occluded by snaring the tapes around the vessels to reduce preload, which caused a gradual decrease in stroke volume (SV) and RV CSA. The snares were released when systolic radial artery pressure reached 70 mm Hg.

Data acquisition and analysis
Echocardiographic images were acquired from the transgastric RV mid–short-axis plane at the LV mid–papillary muscle level as an anatomic landmark (Fig 1) using a Hewlett-Packard Sonos 2500 echocardiographic system (model M2406A; Hewlett-Packard, Andover, MA) with ABD capabilities. A region of interest was then drawn manually immediately beyond the RV endocardial border to exclude the LV cavity and low-density ultrasound signals that may appear within the lateral myocardium.



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Fig 1. Transesophageal echocardiographic cross-sectional view of the right ventricle at the mid–papillary muscle level of the left ventricle. Automated border detection outlines the blood–tissue interface, and the region of interest is drawn around the right ventricular cavity. On-line measures of right ventricular cross-sectional area appear in the graph at the bottom.

 
The analog signals of RV CSA and volumetric flow waves were digitized on-line at 200 Hz with an analog-to-digital converter (MacLab System; AD Instruments, Ltd, Dunedin North, New Zealand) and recorded on a laptop computer (Macintosh Power Book 550C; Apple Computer, Inc, Cupertino, CA). In addition, electrocardiographic lead II signals and radial artery, pulmonary artery, RV, and left atrial pressures were digitized. The SV of each heart beat was calculated by the time integral of the instantaneous volumetric flow of the main pulmonary artery. The stroke area (SA) of each heart beat was calculated as the difference between the maximal and minimal area of each heart beat.

Linear regression analysis was performed to determine the relation between SA and SV during each caval occlusion run. In addition, multiple regression analysis was performed to include all data [10].

Assessment of right ventricular contractility in the intensive care unit
This study group included 14 patients (11 men, 3 women; mean age, 54 ± 15 years [range, 20 to 73 years]) who had undergone open-heart surgical intervention. The operations performed were closure of an atrial septal defect in 2 patients; closure of an atrial septal defect and mitral valve repair in 1 patient; mitral valve replacement and tricuspid annuloplasty in 2 patients; mitral valve repair and tricuspid annuloplasty in 4 patients; closure of an atrial septal defect, mitral valve repair, and the Maze procedure in 1 patient; aortic valve replacement in 3 patients; and aortic valve replacement and the Maze procedure in 1 patient. Mean aortic cross-clamp and cardiopulmonary bypass time was 116 ± 61 and 166 ± 71 minutes, respectively. After operation, patients were transferred to the intensive care unit and connected to a respirator. The setting of the ventilator was unchanged (fraction of inspired oxygen, 0.40 to 0.70; inspiration-expiration ratio, 1:2; positive end-expiratory pressure, 1 to 4 cm H2O) throughout the protocol for each patient. An omniplane transesophageal echocardioscope was inserted as previously described. Once the image had been established, the same region of interest and gain settings were maintained throughout the protocol for each patient. The start of the protocol was approximately 5 hours after removal of the cross-clamp. According to our normal clinical practice, inotropic drugs were given early after operation. Cardiotonic and vasoactive agents administered during the study period were dopamine (dose ranges 0 to 10 µg · kg-1 · min-1; mean, 2.9 µg · kg-1 · min-1) and isosorbide dinitrate (dose range, 0 to 1.9 µg · kg · -1 · min-1; mean, 0.76 µg · kg-1 · min-1) and were unchanged throughout the protocol for each patient. The patients also received an average dosage of dobutamine of 2.1 µg · kg-1 · min-1 before the start of the protocol. Four patients required no inotropic support; 2 patients received dopamine only (2 µg · kg-1 · min-1); 2 patients received dobutamine only (2 and 10 µg · kg-1 · min-1); and 6 patients received both dopamine (range, 2 to 7 µg · kg-1 · min-1; mean, 4.2 µg · kg-1 · min-1) and dobutamine (range, 1 to 5 µg · kg-1 · min-1; mean, 3.8 µg · kg-1 · min-1).

Protocol
After adequate placement of the transesophageal echocardioscope, thermodilution cardiac output was measured, and RV CSA and pressures were recorded simultaneously to obtain steady-state baseline heart beat data. An intravenous nitroglycerin bolus (0.05 to 0.1 mg) was administered to obtain multiple P-A loops with different preloads. An attempt was made to reduce RV peak pressure by 15% during nitroglycerin injection. Studies were repeated after increasing baseline dobutamine dosage by 3 µg · kg-1 · min-1.

Data acquisition and analysis
Right ventricular, left atrial, radial artery, pulmonary artery, and central venous pressures, along with the carbon dioxide concentration of the expiratory gas waveform and electrocardiographic (lead II) signals, were monitored on a bedside monitor (model M1166A; Hewlett-Packard, Inc, Sunnyvale, CA). All these signals and the analog RV area signal from the echocardiograph were digitized on-line and recorded as previously described. The RV pressure and area signals were plotted to display P-A loops in real time. It has been shown that there is a delay in area signal output because of the time required for calculating area on the echocardiograph [9]. Our preliminary study directly comparing ventricular volume and area signal showed that the delay was 40 ms. To synchronize RV pressure data with the area data from the echocardiographic ABD system, we advanced the RV area signal by 40 ms in all patients.

From the steady-state beats, maximal CSA (Amax) and minimal CSA (Amin) were obtained. The SA (Amax - Amin) and fractional area change (SA/Amax) were calculated. The SA and fractional area change are the echocardiographic surrogates of SV and RT ejection fraction, respectively. The end-systolic elastance (Ees) and area axis intercept of the ESPAR were obtained as follows: To eliminate the effects of positive pressure ventilation during the nitroglycerin bolus injection (0.05 to 0.1 mg), only the data during end-expiratory periods were selected using the "cut-and-paste" function of the MacLab system for the analysis. The data obtained underwent an iterative process previously described to obtain Ees and area axis intercept [11]. To determine the position of the ESPAR in the operating range, the area associated with an end-systolic pressure of 25 mm Hg (A25) was calculated as A25 = A0 + 25/Ees, where A0 is the area axis intercept.

The effective arterial elastance of the pulmonary artery was calculated as the ratio of end-systolic pressure to SA. The coupling between the right ventricle and pulmonary artery was determined by calculating Ees. The total mechanical energy generated by ventricular contraction, defined by the pressure–volume area, was defined as the area circumscribed by the end-systolic trajectory of the P-A loop, the end-systolic P-A line, and the end-diastolic P-A relation. External work was calculated as the area inside the P-A loop and is equivalent to stroke work. The efficiency of energy transfer from the ventricle to the arterial system was evaluated as the ratio of external work to the pressure–volume area.

Statistics
Results are presented as mean value ± standard deviation. A paired t test was performed to compare the variables at baseline and in response to increased dobutamine infusion. An analysis of covariance was applied to compare the ESPAR regression lines between baseline values and the presence of the increased dobutamine infusion, in which dummy variables were coded for patient number and the presence of the increased dose of dobutamine [12]. A p value less than 0.05 was considered statistically significant. For all statistical analyses, SPSS (version 6.1J for the Macintosh) was used.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Right ventricular cross-sectional area by automated border detection versus stroke volume
A representative recording of the pulmonary artery flow signal, area signal, and other hemodynamic data during caval occlusion is shown in Figure 2. The correlation coefficient between SA and SV in this representative run was 0.903 (Fig 3). The relations between SA and SV for 8 individual patients after cardiopulmonary bypass are summarized in Table 1. For these runs, a linear relation was observed between SA and SV, with an average correlation of r = 0.933 ± 0.023. Multiple linear regression analysis, including all data (80 pairs of SA and SV), showed that the relation between SA and SV was highly significant (r = 0.952; p < 0.0001).



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Fig 2. Example of simultaneous right ventricular pressure, pulmonary artery flow signal, cross-sectional area waveform, and other hemodynamic variables during vena caval occlusion and release.

 


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Fig 3. Relation between stroke area (maximal cross-sectional area minus minimal cross-sectional area) and stroke volume in a patient after cardiopulmonary bypass.

 

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Table 1. Results of Linear Regression Analysis to Determine the Relation Between Stroke Area and Stroke Volume by Automated Border Detection

 
Assessment of right ventricular contractility in the intensive care unit
All patients had achieved hemodynamic stability in the intensive care unit at the time of the study. Representative RV P-A loops with the slope of the ESPAR at baseline and with increasing the dosage of dobutamine obtained by the intravenous nitroglycerin bolus are shown in Figure 4. Figure 5 shows the changes in variables obtained from RV P-A loops after increasing the dosage of the dobutamine infusion. As a group, there was an increase in Ees (from 4.56 ± 2.42 to 7.34 ± 3.62 mm Hg/cm2, p < 0.01), no change in Ea effective arterial elastance (from 8.70 ± 3.39 to 8.91 ± 3.28 mm Hg/cm2, not significant, and a decrease in the coupling ratio of effective arterial elastance to Ees (from 2.65 ± 1.99 to 1.60 ± 1.21, p < 0.01), which resulted in an increase in the ratio of external work to the pressure-volume area (from 0.41 ± 0.15 to 0.50 ± 0.16, p < 0.01). The increase in this ratio indicates an improvement in the energy transfer from the ventricle to the arterial system. With increased dobutamine infusion, the area associated with an end-systolic pressure of 25 mm Hg significantly decreased (from 7.3 ± 3.5 to 5.6 ± 3.6 cm2, p < 0.01), whereas the area axis intercept remained unchanged (from -0.6 ± 5.9 to 1.2 ± 3.6 cm2, p = no significant difference).



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Fig 4. Representative recordings of right ventricular (RV) pressure–area relations showing the end-systolic pressure–area relation at baseline and with increasing dosage of dobutamine (diagonal lines). There was an increase in right ventricular end-systolic elastance with augmented dobutamine infusion.

 


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Fig 5. Changes in end-systolic elastance (Ees), the intercept of the end-systolic pressure–area relation (A0), the area associated with the end-systolic pressure of 25 mm Hg (A25), effective arterial elastance (Ea), the ratio of effective arterial elastance to end-systolic elastance (Ea/Ees), and the efficiency of energy transfer from pressure–volume area to external work (EW/PVA) at baseline and in response to increasing dosage of dobutamine infusion. Mean values ± standard deviation are also shown. (n.s. = not significant.)

 
Hemodynamic variables obtained from baseline RV pressure and RV CSA are shown in Table 2. With increased dobutamine infusion, there were increases in peak RV pressure (from 28.0 ± 5.4 to 33.4 ± 5.0 mm Hg, p < 0.01), end-systolic RV pressure (from 24.9 ± 4.5 to 29.1 ± 8.1 mm Hg, p < 0.01), maximal rate of increase of RV pressure (from 212.6 ± 65.7 to 302.9 ± 127.7 mm Hg/s, p < 0.01), and fractional area change (from 37.4% ± 13.7% to 43.8% ± 16.0%, p < 0.05) and a decrease in the minimal CSA (from 6.3 ± 3.7 to 5.4 ± 3.4 cm2, p < 0.01). There were no significant changes in end-diastolic RV pressure (from 5.2 ± 2.3 to 5.5 ± 2.3 mm Hg, p > 0.05), maximal CSA (from 9.5 ± 4.3 to 8.9 ± 3.9 cm2, p > 0.05), and SA (from 3.2 ± 1.3 to 3.5 ± 1.1 cm2, p > 0.05).


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Table 2. Hemodynamic Variables Obtained From Baseline Right Ventricular Pressure and Cross-Sectional Area at Baseline and With Increased Dobutamine Infusion

 
Hemodynamic variables obtained from the rapid-response thermodilution catheter are shown in Table 3. A predicted significant increase in cardiac output, SV, heart rate, mean aortic pressure, mean pulmonary artery pressure, LV stroke work, RV stroke work, and RV ejection fraction occurred with the increase in dobutamine dose. Systemic vascular resistance decreased significantly. No significant changes in left atrial pressure, central venous pressure, and pulmonary vascular resistance were observed.


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Table 3. Hemodynamic Variables Obtained from the Rapid-Response Thermodilution Catheter

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
In the present study, we were able to elucidate the alteration in RV contractility by demonstrating RV P-A loops in patients in the intensive care unit. A small incremental dose of dobutamine caused increases in the slope of the RV ESPAR. Validation of using the RV CSA as a surrogate for volume was accomplished in the operating room by simultaneously measuring the volumetric flow of the pulmonary artery. There was a close correlation between the RV SA measured by transesophageal echocardiography and the RV SV obtained from the electromagnetic flow meter. The method of assessing RV contractility appeared to be well applicable in both the operating room and the intensive care unit.

Measurement of ventricular volume is mandatory for the assessment of ventricular function. Previously reported methods to measure ventricular volume, including standard angiography [13], multiple marker technique [14], radionuclide ventriculography [15], and three-dimensional echocardiography [3], require substantial off-line analysis. In addition, most of these methods have limitations to their use in the operating room. Use of a conductance catheter is a standard method for obtaining on-line LV volume signal [16]. However, using a conductance catheter to measure RV volume is controversial because of the complex geometry of the RV [12, 17]. The conductance catheter method has not been validated in the human right ventricle. The use of transesophageal echocardiography equipped with ABD capability is an ideal tool for the on-line estimation of ventricular volume in surgical patients, provided that the RV area closely reflects RV volume. Gorcsan and colleagues [9] performed an intraoperative study using ABD to assess LV function in patients undergoing coronary artery bypass grafting. They demonstrated a close correlation between LV SA measured by ABD and SV obtained by flow meter [18]. In the current study, a similar close correlation was found between the RV SA and SV.

Previous studies of LV function have extensively discussed the limitations of ABD using CSA as a surrogate for volume [7, 9, 18]. Such limitations include the need for images of good quality, subjective adjustment of ultrasound variables, and assurances that observers are reviewing identical cross-sectional images. In addition, the complex geometry of the right ventricle, as well as abnormal function and loading conditions, may alter the relation between CSA and RV volume. In our study, the task of operating transesogeal echocardiographic probe was assigned to one person (Y.O.) to obtain uniformity of RV images. The images were obtained by first visualizing the short-axis view of the left ventricle through the transgastric approach and then by rotating the probe to visualize the right ventricle without the tricuspid or pulmonary valve. This technique limited the cross-sectional plane, which helped to standardize the cross-sectional view of the right ventricle. In addition, we did not alter the ultrasound variables once the experimental protocol had started.

Using an isolated heart preparation, Oe and colleagues [19] studied the relation between RV CSA detected by ABD and RV volume measured directly by placing an intraventricular balloon in the right ventricle. Although there were conformational alterations that caused small changes in CSA during isovolumetric contraction, they showed a highly linear correlation between RV CSA and volume. In our study, the SA–SV relation was acceptably linear. We agree with the argument that linear correlation between SA and SV does not guarantee the use of CSA as a surrogate for volume because (1) it does not directly compare CSA and volume; and (2) there was a patient-to-patient variation in the SA–SV relation in our study. Variation in RV geometry because of underlying disease may be the cause of patient-to-patient variation in the SA–SV relation. Thus it should be emphasized that observations using this method should be limited to measuring serial changes in the same subject. It should also be mentioned that the condition of the patient, such as open or closed, chest may alter RV geometry and may affect the relation between RV CSA and volume. Furthermore, previous observations of discrepancy between the variables of RV function obtained from long- and short-axis views indicated the need for additional studies to verify the use of CSA as a surrogate for RV volume [20]. To clarify these issues, instantaneous and simultaneous measurement of RV volume and CSA should be performed. Unfortunately, no methodology is currently available to fulfill this requirement, especially in the operating room and intensive care unit.

We used an intravenous nitroglycerin bolus to alter loading conditions to obtain multiple P-A loops. On-line acquisition of pressure and area data made it possible to use all data obtained during the decline in pressure to determine the ESPAR. The effect of the respirator was eliminated by selecting the beats during the end-expiratory period. Except for the study in the operating room using vena cava occlusion to alter the preload [2], previous studies [12, 14] used pharmacologic (nitroglycerin or phenylephrine) or volume challenge to obtain alterations in loading conditions. In those studies, however, the number of the end-systolic points was limited to two or three at most because one pharmacologic or volume challenge was required to obtain one end-systolic point. Accordingly, the time required to obtain one ESPVR was lengthy. In our method, the ESPAR was constructed from 5 to 10 end-systolic points, and the time to acquire the ESPAR required only a few minutes. The short acquisition time allowed us to perform multiple interventions in a short period of time. For postoperative patients with hemodynamic instability, the short time required for the study was an advantageous factor.

The changes observed in RV ESPAR during the dobutamine infusion were comparable to previous findings in the left ventricle (ie, the increase in the slope of the ESPVR) [16]. Reports on RV function are limited, however. Maughan and colleagues [21] showed in a canine isolated heart preparation that the ESPVR was linear and that the slope of the ESPVR increased with inotropic intervention. Human studies using radionuclide angiography to determine the RV ESPVR showed an increase in the slope of the RV ESPVR as well [15]. Gorcsan and colleagues [1] used transthoracic echocardiography with ABD to elucidate the RV ESPAR in the catheterization laboratory. They used a balloon catheter to occlude the inferior vena cava to alter preload, thereby obtaining multiple P-A loops. In their patients with end-stage heart failure, they reported similar results with dobutamine infusion. In our study, we were able to elucidate the expected physiologic RV response with a small incremental dobutamine dosage and less invasive intervention.

The potential application of this method is immense because of its availability in the operating room and intensive care unit. The method is especially useful in patients who require separate assessment of RV contractile function and RV afterload because conventional functional variables such as RV ejection fraction and RV stroke work are afterload dependent. Patients with pathologic RV function or pulmonary circulation, including those with congenital heart disease with RV hypertrophy, patients with pulmonary hypertension undergoing lung transplantation, and patients requiring an LV assist device, are the candidates for investigation by this transesophageal echocardiographic method. Assessment of the myocardial protection of the right ventricle is another area in which application of this method is considered feasible. Further study is warranted to demonstrate the applicability of ABD for elucidating RV load-independent variables in the operating room and intensive care unit.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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