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investigations .clinical .... ..-------------Transesophageal Echocardiographic Findings in Patients with Orthotopic Heart Transplantation* Gerardo Polanco, M.D.; Syed AI. Jafn, M.D.; Mohsin Alam, M.D., F.C.C.P.; and T: Barry Levine, M.D.
This study was performed to determine the diagnostic value of TEE in recipients of orthotopic heart transplantation. Findings on TEE were compared with those of TTE in 30 patients with orthotopic heart transplantation. Transesophageal echocardiography identified left atrial appendage and Row across the interatrial septum . . . findings not detected by TTE. In addition, pronounced bulging of the interatrial septum was seen in six patients by TEE and not by TTE. Spontaneous echo contrast (smoke) in the atria was detected by TEE in 14 patients and by TTE in one patient. Abnormal geometry of the atria and donor-recipient atrial anastomosis was identified in all patients by TEE and TTE. Our findings
transplantation is an established therapeutic C ardiac option in the management of end-stage heart
failure. Rejection, graft atherosclerosis and infection remain the major causes for morbidity and mortality in these patients. Heart failure due to myocardial infarction secondary to coronary occlusive disease is becoming another cause for morbidity and mortality in these patients. The frequency of systemic embolization in heart transplant recipients who develop left ventricular dysfunction is unknown. 1 The increased size of the atria following heart transplantation can promote stasis and thrombus formation. We recently have detected the presence of atrial thrombi on TTE and systemic thromboembolism in association with heart failure as another complication in these patients. Transesophageal echocardiography has been shown to be superior to TTE in delineating cardiac anatomy and identifying thrombi" in other cardiac conditions. Echocardiography utilizing the M-mode, two-dimensional and Doppler studies have been shown to be useful in determining cardiac anatomy, chamber size, hemodynamics and predicting rejection episodes in recipients of heart transplantation.t" There is little information on the utility of TEE in patients with *From the Henry Ford Heart and Vascular Institute, Henry Ford Hospital, Detroit. Manuscript received June 10; revision accepted September 3. Reprint requests: Dr. Alam, Henry Ford Hospital, 2799 West Grand, Detroit 48202
suggest that TEE operating room, in and in those with volume overload anastomosis.
should be selectively utilized in the patients with suspected atrial thrombi, clinically significant right ventricular to assess integrity of interatrial (Chest 1992; 101:599-6(2)
=
= =
LA left atrium, atrial; LAD left atrial dimension; LVDd = left ventricular diastolic dimension; LVEF = left ventricular ejection fraction; LVFS left ventricular fractional shortening; RA right atrium, atrial; TEE = transesophageal echocardiography; TTE transthoracic echocardiography
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=
orthotopic cardiac transplantation. The purpose of this study was to compare the diagnostic utility of both TEE and TTE in delineating the anatomic structures in this patient population and to place these findings in a clinical perspective. METHODS
Patient Population The study group consisted of 30 recipients of orthotopic cardiac transplantation. Twenty-five of these were men with a mean age of 47 ± 8 years. The average time from cardiac transplantation was 25 ± 12 months. All patients were receiving immunosuppressive therapy including cyclosporine, azathioprine and prednisone. In addition, all patients were receiving antiplatelet therapy with aspirin. Hypertension was present in 22 of these patients requiring antihypertensive therapy. Congestive heart failure due to graft coronary artery disease with myocardial infarction was documented in two of these patients.
Echocardiographu Transthoracic M-rnode and two-dimensional echocardiograms were performed using a Hewlett Packard (model 77020 AC) ultrasound system with 2.5-MHz phased array transducers. The heart was imaged in all the standard projections. Chamber size and LVFS were measured by M-mode eehocardiography according to recommendations of the American Society of Echocardiography. fi The LVEF was calculated using the apical four-chamber view The enddiastolic and end-systolic frames were identified and endocardial edge was traced. Ventricular volumes were calculated using the single plane area length method. 7 Doppler and color 00\\' were used to assess valve function and the presence of interatrial shunts. After obtaining informed consent, TEE was performed using a CHEST / 101 / 3 / MARCH, 1992
599
5- M liz phased a rray imaj!inj! transducer mounted on the distal tip ofa 100-cm sinj!lt· plane j!astrosmpe (Hewlett-Packard model 21352A). All patients received a local anesthetic spray prior to the introduction of the transducer. Standard TEE projections were obtained in all the patients.' Color How Doppler examination was used to evaluate the presence of valvular regurgitation and the interatrial septum also was studied lilr the presence of shunts. Spontaneous echo contrast was defined as douds of echoes with swirling motion." Smoke was easily differentiated from white noise echo bv decreasing th e j!ain settings until the excessive j!ain echoes. usuall\: located throughout the ultrasound field . disappeared and then the characteristic swirlinj! How pattern was optimally visualized . Spontaneous echo contrast was graded as mild if it was not very dense and occupyiru; < 40 percent of the atrial cavity. Severe smoke was considered present if it was dense and occupied >40 percent oftbe atrial cavity. All studies were independently reviewed by two echocardlographer s and differences in interpretation were resolv ed by consensus.
Statistical Analys~~ Abnormal findings on TIE and TEE were compared by a McNemar's test, taking into account that the two procedures were conducted on the same patient. 'Io compare the subgroups of patients with smok e found by TEE . analysis of variance was used . Different variables were compared by a likelihood ratio chi square test. A p value :50.05 was considered statistically significant. RESULTS
Cardiac Anatomy Both TTE and TEE identified atrial enlargement, the donor-recipient atrial anastomosis and the abnormal geometry of both atria. Transesophageal echocardiography was superior in demonstrating the LA appendage (p
FIGURE 1. Transesophageal echocardiogram in a heart transplant recipient demonstrating presence of flow across the interatrial septum. S = shunt across interatrial communication.
Shunts and Valvular Regurgitation The presence of a left-to-right shunt across the interatrial anastomosis was detected by TEE in two patients (Fig 1) but not by TTE . Tricuspid regurgitation was documented by TTE in 19 and TEE in 22 patients (p = NS). Mitral regurgitation was detected more frequently by TEE (p
Thrombi and Spontaneous Echocontrast Left atrial thrombus was seen in one patient, who subsequently died after the LA thrombus embolized and caused obstruction of the left ventricular outflow tract. While both TTE and TEE detected the throm-
Table 1- Comparison between Transesophageal and
Transthoracic Echocardiography
Clinical Features
TIE (No .)
LA suture line LA appendage LA smoke LA thrombus RA suture line RA smoke RA thrombus Bulj!ing of at rial septum (donor) Bulging of atrial septum (recipient) Mitral valve prolapse Interatrial shunt Mitral regurgitation Tricuspid regurgitation
16
18
1 1
27 14 1
o
14
600
o 6
1
o o 1
o 9
19
TEE (No .)
9
1 6 5 3
2 16 22
p
Value NS
<0.001 <0.001 NS NS
<0.001
NS
<0.05
NS NS NS
<0.01 NS
FIGURE 2. Tranesophageal echocardiogram in a heart transplant recipient showing left atrial thrombus. T = thrombus.
Transesophageal Echocardiography in Heart Transplantation (Polanco, at aJ)
Table 2-Characteristics of Patientswith and without Atrial Smoke Characteristics
Absent
Mild
Severe
Patients (No.) Age (yr) Donor age (yr) Time from transplant (months) Hypertension (No.) Sinus rhythm (No.) Right atrial pressure (mm Hg) Pulmonary artery systolic pressure (mm Hg) Pulmonary capillary wedge pressure (mm Hg) Cardiac index (L'min/M'')
16 46±9 24±9 27±8
II 51±4 23±10 23±14
3 5O±13 28±8 36±O*
12 16 4±3
II
4±2
26±6
25±4
8.5±3.1
8.9±2.3
14.3±7.8*t
3.2±0.6
3±1
2.3±0.7
9
I 3 10± 11*
36±6
*p
bus, a better definition of the thrombus size and mobility was shown with TEE (Fig 2). Right atrial thrombus was seen by both methods in one patient. The presence of atrial smoke with use of TEE was documented and its severity graded into three groups (absent, mild or severe). In 16 patients, smoke was not detected; in 11 it was mild, while in three patients it was severe. There were no differences in the mean donor age, hypertension or sinus rhythm among the three groups (Table 2). The severe group had their transplantation earlier when compared with the mild group (p
This study shows that both TTE and TEE are complementary in the evaluation of patients with Table 3-Comparison ofEchocardiographic Findings in Patients with and without Atrial Smoke
Patients (No.) LAD (mm) LVDd(mm) LVFS(%) LVEF(%) Atrial thrombi (No.)
Absent
Mild
Severe
16 44±8 47±5 29±6 58±6
II 48±9 46±6 25±9 57±5
3 54±13 53±8 31±15 37± 10·
o
o
*p
2
orthotopic heart transplantation." By TEE a better imaging of atria, the LA appendage and interatrial septum was seen when compared with TTE. Furthermore, only by TEE color flow Doppler were we able to identify left-to-right flow across the area of interatrial anastomosis. Spontaneous echo contrast was seen more frequently by TEE compared with TTE. One preliminary report by Angermann et alii also documented a higher prevalence of atrial smoke and atrial thrombi by TEE in these patients not seen with TTE. In addition, they also described pronounced bulging of the interatrial septum and a higher frequency of valvular regurgitation by TEE. Our findings confirm these previous observations and extend the utility of TEE in also documenting flow across the interatrial anastomosis. The presence of spontaneous echo contrast (smoke) has been reported in patients with mitral valve disease, LA enlargement and atrial fihrillation.v-!' The heart transplant population by the nature of the transplant surgery are left with larger atria. In addition, the abnormal contractile pattern of the atria also could promote stasis. This promotes stasis within the atria and could account for the higher prevalence of atrial smoke (48 percent) in these patients. The clinical significance of "atrial smoke" detected by TEE has not been defined by prospective studies. Castello et al 12 reported that smoke in the atria occurs in 20 percent of patients undergoing TEE and its presence is not related to thrombi identified by this technique. However, other studies suggest that the presence of atrial smoke is related to atrial emboli and identifies patients at an increased thromboembolic risk." There need to be more data demonstrating that atrial smoke is associated with the development of atrial thrombus. Among patients with a severe degree of atrial smoke, two had atrial thrombi and one had an embolic event. These patients also had associated left ventricular dysfunction documented by abnormal hemodynamics and a decreased LVEF. The significance of the presence and degree of smoke detected by TEE needs to be evaluated by long-term prospective studies. Echocardiographic evidence for right ventricular volume overload resulting in tricuspid regurgitation has been well documented in patients with heart transplantation.!' Organic heart disease such as myxomatous degeneration of the tricuspid valve of the transplanted heart and severity of pulmonary hypertension prior to the transplantation have been associated with presence of right ventricular volume overload and severity of tricuspid regurgitation. Presence of left-to-right flow across the interatrial anastomosis could also contribute to progressive right ventricular volume overload. This operative complication can be minimized if TEE is utilized in the operating room to assess the integrity of the interatrial anastomosis. CHEST I 101 I 3 I MARCH, 1992
601
In conclusion, our data document the diagnostic potential of TEE. The clinical significance of "severe" atrial smoke in these patients warrants further followup study in a larger sample size to determine its prognostic significance. The clinical significance of mild stroke in the atria in these patients also needs to be defined by prospective long-term studies. Left-toright How across the interatrial anastomosis should be considered as an additional etiology for right ventricular volume overload. Since TEE as a diagnostic procedure has potential for complications, its use in patients undergoing orthotopic cardiac transplantation should be limited to the perioperative period, in defining suspected thrombi in the LA, in patients with left ventricular dysfunction and in those with clinically significant right ventricular volume overload. Its routine use in all recipients of a cardiac transplantation is not recommended.
6
7
8
9
10 11
REFERENCES
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5
Heck CF, Shumway SJ, Kaye M~ The registry of the International Society for Heart Transplantation: Sixth official report 1989. Heart Transplant 1989; 8:271-76 Aschenberg Schluter M, Kremer ~ Schroder E, Siglow ~ Bleifeld W Transesophageal two-dimensional echocardiography for the detection of left atrial appendage thrombus. J Am Coli Cardioll986; 7:163-66 Stevenson L~ Dadourian BJ, Kobashigawa J, Child JS, Clark SH, Laks H. Mitral regurgitation after cardiac transplantation. Am J Cardioll987; 60:119-22 Ciliberto GR, Cataldo G, Cipriani M, Mascarello M, Fatetra F, Gronda E, et al. Echocardiographic assessment of cardiac allograft rejection. Eur Heart J 1989; 10:400-08 Valantine HA, Appleton C~ Halle LK, Hunt SA, Billingham
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ME, Shumway NE, et aI. A hemodynamic and Doppler echocardiographic study of ventricular function in long-term cardiac allograft recipients: etiology and prognosis of restrictiveconstructive physiology. Circulation 1989; 79:66-15 Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1918; 58:1072-83 Feigenbaum H. Echocardiography. 4th ed. Philadelphia: Lea and Febiger, 1986:149-55 Seward JB, Khanderia BK, Oh JK, Abel MD, Hughes ~ Edwards WD, et aI. Transesophageal echocardiography: technique anatomic correlations, implementation, and clinical applications. Mayo Clin Proc 1988; 63:649-80 Daniel WG, Nellessen U, Schroder E, Nonnast-Daniel B, Bednarski ~ Nikutta ~ et aI. Left atrial spontaneous echo contrast in mitral valve disease: an indicator for an increased thromboembolic risk. J Am Coli Cardioll988; 11:1204-11 McAllister HA, Schnee MJM, Radovancevic B, Frazier OR. A system for grading cardiac allograft rejection. Texas Heart Institute J 1986; 13:1-3 Angermann C, Spes C, Stempfte U, Tammen A, Schutz A, Kemkes B, et al, Morphological and functional characteristics of the transplanted heart: transthoracic versus transesophageal echocardiographic findings (Abstract). Circulation 1989; 80 (suppl 11):474 Castello R, Pearson AC, Labovitz AJ. Prevalence and clinical implications of atrial spontaneous contrast in patients undergoing tranesophageal echocardiography. Am J Cardioll990; 65:114953 Garcia-Fernandez MA, Moreno M, Banuelos F. Two dimensional echocardiographic identification of blood stasis in the left atrium. Am Heart J 1985; 109:600-01 Lewen MK, Bryg RJ, Miller L~ Williams GA, Labovitz AJ. Tricuspid regurgitation by Doppler echocardiography after orthotopic cardiac transplantation. Am J Cardioll981; 59:137174
1i'anse8ophageaEchocardography in Heart Transplantation (Polanco, et 81)