- Email: [email protected]
Comparison of transthoracic echocardiography with second harmonic imaging with transesophageal echocardiography in the detection of right to left shunts
be 23% to 32%,9 –11 mostly consisting of vascular complications. Local wound infection has been the most commonly reported infectious complication.12 Bacteremia, however, related to IABP therapy has not been extensively studied and previous studies have focused on complications of IABP without emphasis on infection.13,14 The confusing terminology used in these studies, namely, “sepsis,” “septicemia,” or “fever and bacteremia,” rather than modern definitions, and surgical IABP insertion in some cases, complicates the ability to determine the incidence of true bacteremia and sepsis during IABP therapy.13,14 Evidence as to the risk of infection attributed to IABP arise from outbreaks of Pseudomonas cepacia and Serratia marcescens bloodstream infection, which have been traced to contaminated pressure transducers and water reservoirs.15,16 Another study has shown high rates of positive catheter-tip cultures of various indwelling arterial and venous catheters following open heart surgery.17 The rate of positive IABP catheter-tip cultures was 7.7%, although the rate of clinically significant bacteremia was quite low. Our study shows that a significant proportion of critically ill cardiac patients developed SIRS and fever. This systemic response appeared mainly during the first 48 hours after insertion and may be attributed to the acute medical illness. However, with an indwelling catheter in place, and given the high rates of true bacteremia and sepsis, ruling out infection and administration of empiric antibiotic therapy are mandatory. This is supported by the intriguing finding of bacteremia detected mainly during the first hours after insertion of an IABP. Further study is needed to evaluate the impact of bacteremia on the outcome of IABP-treated patients, preferably by using a multivariate approach and after controlling for the presence of other indwelling vascular catheters, such as central venous, peripheral, and arterial lines. Our study also raises a provocative question as to the need for
antibiotic prophylaxis administration before IABP placement, and possibly, revision of endocarditis prophylaxis guidelines.
1. Rott D, Behar S, Gottlieb S, Boyko V, Hod H. Usefulness of the Killip classification for early risk stratification of patients with acute myocardial infarction in the 1990s compared with those treated in the 1980s. Israeli Thrombolytic Survey Group and the Secondary Prevention Reinfarction Israeli Nifedipine Trial (SPRINT) Study Group. Am J Cardiol 1997;80:859 – 864. 2. Maki DG, Weise CE, Sarafin HW. A semiquantitative culture method for identifying intravenous-catheter related infection. N Engl J Med 1977;296:1305– 1309. 3. Rangel-Frausto MS, Pittet D, Costigan M, Hwang T, Davis CS, Wenzel RP. The natural history of the systemic inflammatory response syndrome (SIRS). A prospective study. JAMA 1995;273:117–123. 4. Braunwald E, Gorlin R, McIntosh HD, Ross RS, Rudolph AM, Swan HJ. Cooperative study on cardiac catheterization. Infectious, inflammatory, and allergic complications. Circulation 1968;37(suppl. 5):1–101. 5. Sande MA, Levinson ME, Lukas DS, Kaye D. Bacteremia associated with cardiac catheterization. N Engl J Med 1969;281:1104 –1106. 6. Shea KW, Schwartz RK, Gambino AT, Marzo KP, Cunha BA. Bacteremia associated with percutaneous transluminal coronary angioplasty. Cathet Cardiovasc Diagn 1995;36:5–10. 7. Clark H. An evaluation of antibiotic prophylaxis in cardiac catheterization. Am Heart J 1969;77:767–771. 8. Samore MH, Wessolossky MA, Lewis SM, Shubrooks SJ Jr, Karchmer AW. Frequency, risk factors, and outcome for bacteremia after percutaneous transluminal coronary angioplasty. Am J Cardiol 1997;79:873– 877. 9. Curtis JJ, Boland M, Bliss D, Walls J, Boley T, Schmaltz R, Flaker G, Anderson SK. Intra-aortic balloon cardiac assist: complication rates for the surgical and percutaneous insertion techniques. Am Surg 1988;54:142–147. 10. Alvarez JM, Gates R, Rowe D, Brady PW. Complications from intra-aortic balloon counterpulsation: a review of 303 cardiac surgical patients. Eur J Cardiothac Surg 1992;6:530 –535. 11. Makhoul RG, Cole CW, McCann RL. Vascular complications of the intraaortic balloon pump: an analysis of 436 patients. Am Surg 1993;59:546 –548. 12. Beckman CB, Geha AS, Hammond GL, Bave AE. Results and complications of intraaortic balloon counterpulsation. Ann Thorac Surg 1977;24:550 –559. 13. Kantrowitz A, Wasfie T, Freed PS, Rubenfire M, Wajszczuk W, Schork MA. Intraaortic balloon pumping 1967 through 1982: Analysis of complications in 733 patients. Am J Cardiol 1986;57:976 –983. 14. Mc Cabe JC, Abel RM, Subramanian VA, Gay WA Jr. Complication of intraaortic balloon insertion and counterpulsation. Circulation 1978;57:769 –773. 15. Villarino ME, Jarvis WR, O’Hara C, Bresnahan J, Clark N. Epidemic of Serratia marcescens bacteremia in a cardiac intensive care unit. J Clin Microbiol 1989;27:2433–2436. 16. Rutala WA, Weber DJ, Thomann CA, John JF, Saviteer SM, Sarubbi FA. An outbreak of Pseudomonas cepacia bacteremia associated with a contaminated intra-aortic balloon pump. J Thorac Cardiovasc Surg 1988;96:157–161. 17. Damen J. The microbiologic risk of invasive haemodynamic monitoring in open-heart patients requiring prolonged ICU treatment. Intens Care Med 1988; 14:156 –162.
Comparison of Transthoracic Echocardiography With Second Harmonic Imaging With Transesophageal Echocardiography in the Detection of Right to Left Shunts Guy Van Camp, MD, Philippe Franken, MD, Patrik Melis, RN, Bernard Cosyns, Danny Schoors, MD, and Jean Louis Vanoverschelde, MD efects in the interatrial septum as well as abnormalities in the pulmonary vascular bed may reD sult in a right to left shunt. Patent foramen ovale can From the Department of Cardiology, AZ VUB, Brussels; and the Department of Cardiology, UCL, Brussels, Belgium. Dr. Van Camp’s address is: Department of Cardiology-AZ VUB, Laarbeeklaan 101, 1090 Brussels, Belgium. E-mail: [email protected]. Manuscript received April 13, 2000; revised manuscript received and accepted June 16, 2000.
1284
©2000 by Excerpta Medica, Inc. All rights reserved. The American Journal of Cardiology Vol. 86 December 1, 2000
MD,
be responsible for cryptogenic stroke in young patients.1–3 A possible cause of unexplained hypoxemia is the presence of abnormal arteriovenous communications in the pulmonary circulation.4 Contrast echocardiography has been shown to be effective in detecting right to left shunts.1–12 Because transesophageal echocardiography (TEE) provides more accurate diagnostic information on posterior localized structures of the heart than transthoracic echocardiography 0002-9149/00/$–see front matter PII S0002-9149(00)01224-8
(TTE), this technique combined with color Doppler or contrast administration is now considered as the method of choice in the diagnosis of patent foramen ovale.3,7–12 Recently, second harmonic imaging was developed to visualize first- and second-generation contrast agents more selectively than the surrounding tissue.13 Harmonic imaging without the use of contrast also enhances the differentiation between the blood pool in the left ventricle and the surrounding tissue due to the partial clearing of artifacts as reverberations.14 –16 We tested the hypothesis that second harmonic imaging during TTE is as accurate as TEE for detecting right to left shunts in a nonselected population using a simple saline-agitated solution. •••
The patient population consisted of 109 consecutive patients (60 men and 49 women, mean age 64.6 ⫾ 14 years) referred to the echo laboratory for transesophageal echocardiographic examination. Motivation for TEE were cerebrovascular accident (n ⫽ 70 [64%]), transient ischemic attack (n ⫽ 13 [11%]), endocarditis (n ⫽ 11 [10%]), valvular heart disease (n ⫽ 5 [5%]), hepatopulmonary syndrome (n ⫽ 4 [4%]), and other illnesses (n ⫽ 6 [6%]). The presence of atrial fibrillation was established on the electrocardiogram and on 24-hour Holter monitoring. Patients referred for the exclusion of an hepatopulmonary syndrome were patients with end-stage liver disease who presented with unexplained hypoxemia. They all gave informed consent. All transesophageal echocardiographic studies were performed with a Toshiba Powervison 7000, and TTE with fundamental mode and second harmonic modes was performed on a Toshiba Powervison 6000 using broad-band transducers with modalities for second harmonic imaging (2.1/4.2 MHz). In all patients the study began with a complete transesophageal echocardiographic study with a multiplane transesophageal echocardiographic probe. Contrast injections were performed at low dynamic range and relative high gain settings to visualize even the most discrete contrast passage. Before the contrast injections were performed attention was given to the presence of spontaneous and “snowstorm” contrast at these echo settings.17 At least 5 minutes after the disappearance of the bubbles injected during TEE, images of the TTE were stored. First contrast images were performed in fundamental mode. After the disappearance of all contrast bubbles, a second harmonic imaging was performed. In each imaging modality, 3 contrast injections of an agitated 10-ml physiologic saline solution were rapidly administrated through a right antecubital vein using an 18-gauge venous cannula. Each injection was administered just before the release phase of the Valsalva maneuver. The presence of an atrial septal defect or a patent foramen ovale was defined as the passage of contrast in the left cavities within the first 3 cardiac cycles after opacification of the right atrium. When contrast is seen in the left cavities after ⬎3 cardiac cycles, it is considered as a passage of contrast through pulmonary arteriovenous malformations. Right to left shunt was considered important when ⬎20 microbubbles could be visualized.2,5 Image quality was scored from 0 to 2. Image
TABLE 1 Shunting in Fundamental Mode, Second Harmonic Mode, and TEE
Early ⬍20 Early ⬎20 Late
Fundamental Mode (no.)
Second Harmonic Mode (no.)
TEE (no.)
1 8 2
4 17 3
9 12 3
⬍20, ⬎20 ⫽ ⬍20 microbubbles, ⬎20 microbubbles present on one video image in the left cavities.
quality was scored 0 when the estimation of bubble presence was considered very difficult. A score of 1 was given when the image quality allowed one to observe the presence or absence of bubbles without reasonable doubt, but still with image-containing artifacts. A score of 2 was given when perfect delineation of the endocardial borders, the valves, and the interatrial septum was seen. All studies were analyzed off-line from videotapes. Fundamental mode, second harmonic mode, and transesophageal echocardiographic images were read separately and in a random order to avoid bias. Because the difference in image characteristics is obvious, it is not possible to blind the reader to the presence of a fundamental versus second harmonic mode image. Two independent readers estimated the contrast images, and if there was no agreement, a third reader was asked and a consensus was achieved. Numerical results are given as mean ⫾ SD. For the comparison of percentages and proportions (pathologic findings in the stroke patients), the Fisher’s exact test was used. The Wilcoxon paired test was used to compare differences in mean image quality, severity, and timing of contrast. All tests were 2-tailed and a p value ⬍0.05 was considered as significant. Taking into account every contrast passage from the right to left cavities, the fundamental mode detected significantly less shunts than the second harmonic mode and TEE: fundamental mode, 11 of 109 (10%); second harmonic mode, 24 of 109 (22%); and TEE, 24 of 109 shunts (22%) (p ⬍0.05) (Table 1). There was no significant difference between second harmonic mode and TEE for detecting right to left shunts. The fundamental mode detected less patients in each group than the 2 other modalities. Important and early shunting was more often diagnosed by a second harmonic mode than by a fundamental mode and TEE: 17 of 109 (16%) versus 8 of 109 (7%) (p ⬍0.05) and 12 of 109 (11%) (p ⬎0.05). Two of the patients with important shunting on the second harmonic mode had no shunting at all by TEE. Three other patients with important early shunting on the second harmonic mode had poor shunting by TEE. On the other hand, TEE detected a poor (⬍20 bubbles) early shunt in 9 of 109 patients (8%), and a second harmonic TTE detected a poor early shunt in only 4 of these 109 patients (4%). One patient with an important (⬎20 bubbles) early shunt detected by TEE had only a poor early shunt (⬍20 bubbles) with a second harmonic TTE. Three patients with a poor and early shunt detected with TEE had no shunting at all by the second harmonic BRIEF REPORTS
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monic mode in all but 2 patients (mean score 1.9). In the group with contrast passage in the fundamental mode, the image quality was already excellent in fundamental mode in 9 of 11 patients, and moderate in 2 (mean score 1.8) (p ⬍0.05). •••
FIGURE 1. Contrast study in a patient. Top, no contrast passage visible in fundamental mode (clutter and nonmoving artifacts are clearly visible in the left ventricular cavity; endocardial border delineation is not clear). Middle, clearly visible contrast bubbles in the left ventricle with almost no clutter in second harmonic mode (clear endocardial border definition). Bottom, no passage visible in the transesophageal echocardiographic image in the transverse (and longitudinal [not shown]) view (excellent image quality).
mode. Three patients with ⬍20 bubbles early shunting by TEE had no shunting at all by the second harmonic mode. The separation of early and late contrast passage was completely concordant between fundamental mode, second harmonic mode, and TEE (Table 1). An important gain in image quality was obtained from fundamental to second harmonic mode: 1.33 ⫾ 0.72 and 1.87 ⫾ 0.34 (mean score ⫾ SD). The incremental quality gain from second harmonic to TEE was very small, as the mean score for TEE was 1.99 ⫾ 0.10. In second harmonic mode, the image was clearer but the bubbles appeared also brighter and larger than in fundamental mode. In the group without contrast passage in the fundamental mode, although there was a passage proved by second harmonic mode, the image quality was close to moderate in fundamental mode (mean score 1.1) and excellent in second har1286 THE AMERICAN JOURNAL OF CARDIOLOGY姞
VOL. 86
The detection of a right to left shunt at the level of the heart or the pulmonary circulation is of clinical importance in different patient populations. The most important group of patients are those with unexplained stroke. These patients may have a patent foramen ovale, which can act as an open door for thrombotic material coming from legs or pelvis.1–3,6 –11 Also, detecting a patent foramen ovale in divers with a history of decompression sickness is of critical importance.12 Furthermore, abnormal arteriovenous communication may result in right to left shunting, as may be seen in cirrhotic patients or in some congenital abnormalities.4,5 The results of our study can be summarized as follows: Taking into account every contrast passage, the second harmonic mode detected right to left shunting equally as effective as TEE. The same incremental value of the second harmonic versus the fundamental mode was observed as for TEE versus the fundamental mode. Compared with TEE, the second harmonic mode detected important early microbubble passage more often. From the 5 patients “missed” by TEE, 3 had a poor (⬍20 bubbles) and early passage, and the 2 others had no passage at all (Figure 1). On the contrary, TEE detected poor and early shunting in 3 patients. Second harmonic TTE did not show any shunt in these patients. TEE also detected one important early shunting, whereas the second harmonic mode showed only small early shunting. When contrast was detected by an imaging modality, the timing of the contrast passage was identical in the other imaging modalities. We can conclude from these observations that the second harmonic mode and TEE appear to be equally accurate and complementary for detecting these right to left shunts (Table 1). Our results suggest a clear relation between the better image with less artefacts in the second harmonic mode than in the fundamental mode, and a higher detection rate of right to left shunts with the second harmonic mode than with the fundamental mode. It is widely accepted that TEE, with the administration of intravenous contrast and the use of color Doppler, is the reference method for detecting patent foramen ovale.2,3,7–11 However, transcranial Doppler examinations have shown that in some patients TEE may fail to demonstrate right to left shunting in patent foramen ovale.11 Also, in patients with end-stage liver disease, contrast TEE proved to be the method of choice compared with contrast TTE or lung perfusion scintigraphy for detecting abnormal arteriovenous communication.5 Taking into account these considerations, contrast TEE is considered as the reference method for detecting early and late contrast passages in right to left shunting. However, second harmonic imaging was recently introduced in most new TTE machines using broad-band transducers. This imaging modality has DECEMBER 1, 2000
the potential to visualize gas microbubbles better than conventional TTE as a result of 2 characteristics. In the second harmonic mode, most of the clutter inside the cavities, as seen in conventional fundamental mode transthoracic echocardiographic images, is cleared,14 and second harmonic imaging exploits the nonlinear behavior of microbubbles.13 This second harmonic mode technique makes TTE more accurate in the detection of gas microbubbles in the heart cavities and more specifically in the diagnosis of right to left shunts as demonstrated in our study. The most plausible explanation for not detecting the contrast passage by TEE is the difficulty patients have in performing a good Valsalva maneuver because of the presence of the endoscope.9,10 All but 2 patients in our study group stated that the Valsalva maneuver was clearly easier to perform during TTE than during TEE. Ku¨hl and colleagues18 demonstrated the same accuracy of the second harmonic mode for detecting right to left shunting. However, the limitation of this study was the use of a polygelatin solution contrast agent in a selected patient population with cryptogenic stroke. In routine clinical practice, agitated saline solutions are used and our study demonstrated the feasibility and accuracy of saline injections with second harmonic mode TTE to detect right to left shunts in a nonselected population of patients sent to the echo lab for TEE. This study has a major impact on clinical practice. Considering the accuracy to detect the right to left shunts and to give an adequate timing of the shunt, we propose to use second harmonic mode imaging with the use of agitated saline injections as an alternative to TEE. Indeed, TEE can be avoided such as in healthy divers, in whom the only question is if the subject has a patent foramen ovale. Also, TEE can be avoided in cirrhotic patients with a suspicion of a hepatopulmonary syndrome. These patients often have esophageal varicose veins and often need repetitive gastroscopies. TEE is often performed in stroke patients to detect a possible thromboembolic source in the heart or the great vessels.6,819,20 In patients without an underlying cardiomyopathy, the yield of TEE is low compared with fundamental mode TTE, except when detecting patent foramen ovale. In patients with a normal TTE and in sinus rhythm, the TEE findings of a left atrial thrombus, spontaneous contrast in the left atrium, and complex aortic atheroma are extremely rare.19 In our young stroke patient who did not present with an underlying cardiomyopathy or atrial fibrillation, the only detected thromboembolic risk factor was a patent foramen ovale in 7 of the 21 patients. Therefore, in young patients in sinus rhythm and without a history of cardiac disease, second harmonic mode TTE is a tempting technique to replace TEE and thereby avoid a high workload in the echo laboratory. Using hand-agitated saline solutions, second harmonic mode TTE and TEE are equally sensitive
in detecting right to left shunts in patients undergoing a daily routine TEE. Second harmonic mode TTE is able to differentiate late from early contrast passages. Our observations suggest that the second harmonic mode can be used as an alternative for TEE to calculate patent foramen ovale in divers and young stroke patients without underlying heart disease and without atrial fibrillation. In cirrhotic patients it is able to detect the hepatopulmonary syndrome.
1. Lechat P, Mas JL, Lascault G, Loron PH, Theard M, Klimczac M, Drobinski
G, Thoms D, Grosgogeat Y. Prevalence of patent foramen ovale in patients with stroke. N Engl J Med 1988;318:1148 –1152. 2. de Belder MA, Tourikis L, Leech G, Camm AJ. Risk of patent foramen ovale for thromboembolic events in all age groups. Am J Cardiol 1992;69:1316 –1320. 3. Van Camp G, Schulze D, Cosyns B, Vandenbossche JL. Relation between patent foramen ovale and stroke. Am J Cardiol 1993;71:596 –598. 4. Barzilai B, Waggoner AD, Spessert C, Picus D, Goodenberger D. Twodimensional contrast echocardiography in the detection and follow-up of congenital pulmonary arteriovenous malformations. Am J Cardiol 1991;68:1507– 1510. 5. Vedrinne JM, Duperret S, Bizollon T, Magnin C, Motin J, Trepo C, Ducerf C. Comparison of transesophageal and transthoracic contrast echocardiography for detection of an intrapulmonary shunt in liver disease. Chest 1997;111:1236 – 1240. 6. Pearson AC, Labovitz AJ, Tatineni S, Gomez CR. Superiority of transesophageal echocardiography in detecting cardiac sources of embolism in patients with cerebral ischemia of uncertain etiology. J Am Coll Cardiol 1991;17:66 –72. 7. de Belder MA, Tourikis L, Griffith M. Transesophageal contrast echocardiography and color flow mapping: methods of choice for the detection of shunts at the atrial level? Am Heart J 1992;124:1545–1550. 8. Lee RJ, Bartzokis T, Yeoh TK, Grogin HR, Choi D, Schnittner I. Enhanced detection of intracardiac sources of cerebral emboli by transesophageal echocardiography. Stroke 1991;22:734 –739. 9. Devuyst G, Despland PA, Bogousslavsky J, Jeanrenaud X. Complementarity of contrast transcranial Doppler and contrast transesophageal echocardiography for the detection of patent foramen ovale in stroke patients. Eur Neurol 1997; 38:21–25. 10. Sun JP, Stewart WJ, Hanna J, Thomas JD. Diagnosis of patent foramen ovale by contrast versus color Doppler by transesophageal echocardiography: relation to atrial size. Am Heart J 1996;131:239 –244. 11. Nemec JJ, Marwick TH, Lorig RJ, Davison MB, Chimowitz MI, Litowitz H, Salcedo EE. Comparison of transcranial Doppler ultrasound and transesophageal contrast echocardiography in the detection of interatrial right-to-left shunts. Am J Cardiol 1991;68:1498 –1502. 12. Wilmshurst PT, Byrne JC, Webb-Peploe MM. Relation between interatrial shunts and decompression sickness in divers. Lancet 1989;2:1302–1306. 13. Burns PN, Powers JE, Fritzsch T. Harmonic imaging: a new imaging and Doppler method for contrast enhanced ultrasound (abstr). Radiology 1992;185: 142. 14. Thomas JD, Rubin DN. Tissue harmonic imaging: why does it works? J Am Soc Echocardiogr 1998;11:803– 808. 15. Senior R, Soman P, Khattar, RS, Lahiri A. Improved endocardial visualization with second harmonic imaging compared with fundamental two-dimensional echocardiographic imaging. Am Heart J 1999;138:163–168. 16. Pyles JM, Sawada SG, Feigenbaum H, Segar DS. Enhanced endocardial visualization using harmonic imaging without contrast. Cardiovasc Imag 1998; 10:77– 82. 17. Van Camp G, Cosyns B, Vandenbossche JL. Non-smoke spontaneous contrast in the left atrium intensified by respiratory manoeuvres: a new transoesophageal echocardiographic observation. Br Heart J 1994;72:446 – 451. 18. Ku¨hl HP, Hoffmann R, Merx MW, Franke A, Klo¨tzsch C, Lepper W, Reineke T, Noth J, Hanrath P. Transthoracic echocardiography using second harmonic imaging: diagnostic alternative to transesophageal echocardiography for the detection atral right to left shunt in patients with cerebral embolic events. J Am Coll Cardiol 1999;34:1823–1830. 19. de Belder MA, Lovat LB, Tourikis L, Leech G, Camm AJ. Limitations of transoesophageal echocardiography in patients with focal cerebral ischaemic events. Br Heart J 1992;67:297–303. 20. Leung DY, Black IW, Cranney GB. Selection of patients for transesophageal echocardiography after stroke and systemic embolic events. Role of transthoracic echocardiography. Stroke 1995;26:1820 –1824.
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antibiotic prophylaxis administration before IABP placement, and possibly, revision of endocarditis prophylaxis guidelines.
1. Rott D, Behar S, Gottlieb S, Boyko V, Hod H. Usefulness of the Killip classification for early risk stratification of patients with acute myocardial infarction in the 1990s compared with those treated in the 1980s. Israeli Thrombolytic Survey Group and the Secondary Prevention Reinfarction Israeli Nifedipine Trial (SPRINT) Study Group. Am J Cardiol 1997;80:859 – 864. 2. Maki DG, Weise CE, Sarafin HW. A semiquantitative culture method for identifying intravenous-catheter related infection. N Engl J Med 1977;296:1305– 1309. 3. Rangel-Frausto MS, Pittet D, Costigan M, Hwang T, Davis CS, Wenzel RP. The natural history of the systemic inflammatory response syndrome (SIRS). A prospective study. JAMA 1995;273:117–123. 4. Braunwald E, Gorlin R, McIntosh HD, Ross RS, Rudolph AM, Swan HJ. Cooperative study on cardiac catheterization. Infectious, inflammatory, and allergic complications. Circulation 1968;37(suppl. 5):1–101. 5. Sande MA, Levinson ME, Lukas DS, Kaye D. Bacteremia associated with cardiac catheterization. N Engl J Med 1969;281:1104 –1106. 6. Shea KW, Schwartz RK, Gambino AT, Marzo KP, Cunha BA. Bacteremia associated with percutaneous transluminal coronary angioplasty. Cathet Cardiovasc Diagn 1995;36:5–10. 7. Clark H. An evaluation of antibiotic prophylaxis in cardiac catheterization. Am Heart J 1969;77:767–771. 8. Samore MH, Wessolossky MA, Lewis SM, Shubrooks SJ Jr, Karchmer AW. Frequency, risk factors, and outcome for bacteremia after percutaneous transluminal coronary angioplasty. Am J Cardiol 1997;79:873– 877. 9. Curtis JJ, Boland M, Bliss D, Walls J, Boley T, Schmaltz R, Flaker G, Anderson SK. Intra-aortic balloon cardiac assist: complication rates for the surgical and percutaneous insertion techniques. Am Surg 1988;54:142–147. 10. Alvarez JM, Gates R, Rowe D, Brady PW. Complications from intra-aortic balloon counterpulsation: a review of 303 cardiac surgical patients. Eur J Cardiothac Surg 1992;6:530 –535. 11. Makhoul RG, Cole CW, McCann RL. Vascular complications of the intraaortic balloon pump: an analysis of 436 patients. Am Surg 1993;59:546 –548. 12. Beckman CB, Geha AS, Hammond GL, Bave AE. Results and complications of intraaortic balloon counterpulsation. Ann Thorac Surg 1977;24:550 –559. 13. Kantrowitz A, Wasfie T, Freed PS, Rubenfire M, Wajszczuk W, Schork MA. Intraaortic balloon pumping 1967 through 1982: Analysis of complications in 733 patients. Am J Cardiol 1986;57:976 –983. 14. Mc Cabe JC, Abel RM, Subramanian VA, Gay WA Jr. Complication of intraaortic balloon insertion and counterpulsation. Circulation 1978;57:769 –773. 15. Villarino ME, Jarvis WR, O’Hara C, Bresnahan J, Clark N. Epidemic of Serratia marcescens bacteremia in a cardiac intensive care unit. J Clin Microbiol 1989;27:2433–2436. 16. Rutala WA, Weber DJ, Thomann CA, John JF, Saviteer SM, Sarubbi FA. An outbreak of Pseudomonas cepacia bacteremia associated with a contaminated intra-aortic balloon pump. J Thorac Cardiovasc Surg 1988;96:157–161. 17. Damen J. The microbiologic risk of invasive haemodynamic monitoring in open-heart patients requiring prolonged ICU treatment. Intens Care Med 1988; 14:156 –162.
Comparison of Transthoracic Echocardiography With Second Harmonic Imaging With Transesophageal Echocardiography in the Detection of Right to Left Shunts Guy Van Camp, MD, Philippe Franken, MD, Patrik Melis, RN, Bernard Cosyns, Danny Schoors, MD, and Jean Louis Vanoverschelde, MD efects in the interatrial septum as well as abnormalities in the pulmonary vascular bed may reD sult in a right to left shunt. Patent foramen ovale can From the Department of Cardiology, AZ VUB, Brussels; and the Department of Cardiology, UCL, Brussels, Belgium. Dr. Van Camp’s address is: Department of Cardiology-AZ VUB, Laarbeeklaan 101, 1090 Brussels, Belgium. E-mail: [email protected]. Manuscript received April 13, 2000; revised manuscript received and accepted June 16, 2000.
1284
©2000 by Excerpta Medica, Inc. All rights reserved. The American Journal of Cardiology Vol. 86 December 1, 2000
MD,
be responsible for cryptogenic stroke in young patients.1–3 A possible cause of unexplained hypoxemia is the presence of abnormal arteriovenous communications in the pulmonary circulation.4 Contrast echocardiography has been shown to be effective in detecting right to left shunts.1–12 Because transesophageal echocardiography (TEE) provides more accurate diagnostic information on posterior localized structures of the heart than transthoracic echocardiography 0002-9149/00/$–see front matter PII S0002-9149(00)01224-8
(TTE), this technique combined with color Doppler or contrast administration is now considered as the method of choice in the diagnosis of patent foramen ovale.3,7–12 Recently, second harmonic imaging was developed to visualize first- and second-generation contrast agents more selectively than the surrounding tissue.13 Harmonic imaging without the use of contrast also enhances the differentiation between the blood pool in the left ventricle and the surrounding tissue due to the partial clearing of artifacts as reverberations.14 –16 We tested the hypothesis that second harmonic imaging during TTE is as accurate as TEE for detecting right to left shunts in a nonselected population using a simple saline-agitated solution. •••
The patient population consisted of 109 consecutive patients (60 men and 49 women, mean age 64.6 ⫾ 14 years) referred to the echo laboratory for transesophageal echocardiographic examination. Motivation for TEE were cerebrovascular accident (n ⫽ 70 [64%]), transient ischemic attack (n ⫽ 13 [11%]), endocarditis (n ⫽ 11 [10%]), valvular heart disease (n ⫽ 5 [5%]), hepatopulmonary syndrome (n ⫽ 4 [4%]), and other illnesses (n ⫽ 6 [6%]). The presence of atrial fibrillation was established on the electrocardiogram and on 24-hour Holter monitoring. Patients referred for the exclusion of an hepatopulmonary syndrome were patients with end-stage liver disease who presented with unexplained hypoxemia. They all gave informed consent. All transesophageal echocardiographic studies were performed with a Toshiba Powervison 7000, and TTE with fundamental mode and second harmonic modes was performed on a Toshiba Powervison 6000 using broad-band transducers with modalities for second harmonic imaging (2.1/4.2 MHz). In all patients the study began with a complete transesophageal echocardiographic study with a multiplane transesophageal echocardiographic probe. Contrast injections were performed at low dynamic range and relative high gain settings to visualize even the most discrete contrast passage. Before the contrast injections were performed attention was given to the presence of spontaneous and “snowstorm” contrast at these echo settings.17 At least 5 minutes after the disappearance of the bubbles injected during TEE, images of the TTE were stored. First contrast images were performed in fundamental mode. After the disappearance of all contrast bubbles, a second harmonic imaging was performed. In each imaging modality, 3 contrast injections of an agitated 10-ml physiologic saline solution were rapidly administrated through a right antecubital vein using an 18-gauge venous cannula. Each injection was administered just before the release phase of the Valsalva maneuver. The presence of an atrial septal defect or a patent foramen ovale was defined as the passage of contrast in the left cavities within the first 3 cardiac cycles after opacification of the right atrium. When contrast is seen in the left cavities after ⬎3 cardiac cycles, it is considered as a passage of contrast through pulmonary arteriovenous malformations. Right to left shunt was considered important when ⬎20 microbubbles could be visualized.2,5 Image quality was scored from 0 to 2. Image
TABLE 1 Shunting in Fundamental Mode, Second Harmonic Mode, and TEE
Early ⬍20 Early ⬎20 Late
Fundamental Mode (no.)
Second Harmonic Mode (no.)
TEE (no.)
1 8 2
4 17 3
9 12 3
⬍20, ⬎20 ⫽ ⬍20 microbubbles, ⬎20 microbubbles present on one video image in the left cavities.
quality was scored 0 when the estimation of bubble presence was considered very difficult. A score of 1 was given when the image quality allowed one to observe the presence or absence of bubbles without reasonable doubt, but still with image-containing artifacts. A score of 2 was given when perfect delineation of the endocardial borders, the valves, and the interatrial septum was seen. All studies were analyzed off-line from videotapes. Fundamental mode, second harmonic mode, and transesophageal echocardiographic images were read separately and in a random order to avoid bias. Because the difference in image characteristics is obvious, it is not possible to blind the reader to the presence of a fundamental versus second harmonic mode image. Two independent readers estimated the contrast images, and if there was no agreement, a third reader was asked and a consensus was achieved. Numerical results are given as mean ⫾ SD. For the comparison of percentages and proportions (pathologic findings in the stroke patients), the Fisher’s exact test was used. The Wilcoxon paired test was used to compare differences in mean image quality, severity, and timing of contrast. All tests were 2-tailed and a p value ⬍0.05 was considered as significant. Taking into account every contrast passage from the right to left cavities, the fundamental mode detected significantly less shunts than the second harmonic mode and TEE: fundamental mode, 11 of 109 (10%); second harmonic mode, 24 of 109 (22%); and TEE, 24 of 109 shunts (22%) (p ⬍0.05) (Table 1). There was no significant difference between second harmonic mode and TEE for detecting right to left shunts. The fundamental mode detected less patients in each group than the 2 other modalities. Important and early shunting was more often diagnosed by a second harmonic mode than by a fundamental mode and TEE: 17 of 109 (16%) versus 8 of 109 (7%) (p ⬍0.05) and 12 of 109 (11%) (p ⬎0.05). Two of the patients with important shunting on the second harmonic mode had no shunting at all by TEE. Three other patients with important early shunting on the second harmonic mode had poor shunting by TEE. On the other hand, TEE detected a poor (⬍20 bubbles) early shunt in 9 of 109 patients (8%), and a second harmonic TTE detected a poor early shunt in only 4 of these 109 patients (4%). One patient with an important (⬎20 bubbles) early shunt detected by TEE had only a poor early shunt (⬍20 bubbles) with a second harmonic TTE. Three patients with a poor and early shunt detected with TEE had no shunting at all by the second harmonic BRIEF REPORTS
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monic mode in all but 2 patients (mean score 1.9). In the group with contrast passage in the fundamental mode, the image quality was already excellent in fundamental mode in 9 of 11 patients, and moderate in 2 (mean score 1.8) (p ⬍0.05). •••
FIGURE 1. Contrast study in a patient. Top, no contrast passage visible in fundamental mode (clutter and nonmoving artifacts are clearly visible in the left ventricular cavity; endocardial border delineation is not clear). Middle, clearly visible contrast bubbles in the left ventricle with almost no clutter in second harmonic mode (clear endocardial border definition). Bottom, no passage visible in the transesophageal echocardiographic image in the transverse (and longitudinal [not shown]) view (excellent image quality).
mode. Three patients with ⬍20 bubbles early shunting by TEE had no shunting at all by the second harmonic mode. The separation of early and late contrast passage was completely concordant between fundamental mode, second harmonic mode, and TEE (Table 1). An important gain in image quality was obtained from fundamental to second harmonic mode: 1.33 ⫾ 0.72 and 1.87 ⫾ 0.34 (mean score ⫾ SD). The incremental quality gain from second harmonic to TEE was very small, as the mean score for TEE was 1.99 ⫾ 0.10. In second harmonic mode, the image was clearer but the bubbles appeared also brighter and larger than in fundamental mode. In the group without contrast passage in the fundamental mode, although there was a passage proved by second harmonic mode, the image quality was close to moderate in fundamental mode (mean score 1.1) and excellent in second har1286 THE AMERICAN JOURNAL OF CARDIOLOGY姞
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The detection of a right to left shunt at the level of the heart or the pulmonary circulation is of clinical importance in different patient populations. The most important group of patients are those with unexplained stroke. These patients may have a patent foramen ovale, which can act as an open door for thrombotic material coming from legs or pelvis.1–3,6 –11 Also, detecting a patent foramen ovale in divers with a history of decompression sickness is of critical importance.12 Furthermore, abnormal arteriovenous communication may result in right to left shunting, as may be seen in cirrhotic patients or in some congenital abnormalities.4,5 The results of our study can be summarized as follows: Taking into account every contrast passage, the second harmonic mode detected right to left shunting equally as effective as TEE. The same incremental value of the second harmonic versus the fundamental mode was observed as for TEE versus the fundamental mode. Compared with TEE, the second harmonic mode detected important early microbubble passage more often. From the 5 patients “missed” by TEE, 3 had a poor (⬍20 bubbles) and early passage, and the 2 others had no passage at all (Figure 1). On the contrary, TEE detected poor and early shunting in 3 patients. Second harmonic TTE did not show any shunt in these patients. TEE also detected one important early shunting, whereas the second harmonic mode showed only small early shunting. When contrast was detected by an imaging modality, the timing of the contrast passage was identical in the other imaging modalities. We can conclude from these observations that the second harmonic mode and TEE appear to be equally accurate and complementary for detecting these right to left shunts (Table 1). Our results suggest a clear relation between the better image with less artefacts in the second harmonic mode than in the fundamental mode, and a higher detection rate of right to left shunts with the second harmonic mode than with the fundamental mode. It is widely accepted that TEE, with the administration of intravenous contrast and the use of color Doppler, is the reference method for detecting patent foramen ovale.2,3,7–11 However, transcranial Doppler examinations have shown that in some patients TEE may fail to demonstrate right to left shunting in patent foramen ovale.11 Also, in patients with end-stage liver disease, contrast TEE proved to be the method of choice compared with contrast TTE or lung perfusion scintigraphy for detecting abnormal arteriovenous communication.5 Taking into account these considerations, contrast TEE is considered as the reference method for detecting early and late contrast passages in right to left shunting. However, second harmonic imaging was recently introduced in most new TTE machines using broad-band transducers. This imaging modality has DECEMBER 1, 2000
the potential to visualize gas microbubbles better than conventional TTE as a result of 2 characteristics. In the second harmonic mode, most of the clutter inside the cavities, as seen in conventional fundamental mode transthoracic echocardiographic images, is cleared,14 and second harmonic imaging exploits the nonlinear behavior of microbubbles.13 This second harmonic mode technique makes TTE more accurate in the detection of gas microbubbles in the heart cavities and more specifically in the diagnosis of right to left shunts as demonstrated in our study. The most plausible explanation for not detecting the contrast passage by TEE is the difficulty patients have in performing a good Valsalva maneuver because of the presence of the endoscope.9,10 All but 2 patients in our study group stated that the Valsalva maneuver was clearly easier to perform during TTE than during TEE. Ku¨hl and colleagues18 demonstrated the same accuracy of the second harmonic mode for detecting right to left shunting. However, the limitation of this study was the use of a polygelatin solution contrast agent in a selected patient population with cryptogenic stroke. In routine clinical practice, agitated saline solutions are used and our study demonstrated the feasibility and accuracy of saline injections with second harmonic mode TTE to detect right to left shunts in a nonselected population of patients sent to the echo lab for TEE. This study has a major impact on clinical practice. Considering the accuracy to detect the right to left shunts and to give an adequate timing of the shunt, we propose to use second harmonic mode imaging with the use of agitated saline injections as an alternative to TEE. Indeed, TEE can be avoided such as in healthy divers, in whom the only question is if the subject has a patent foramen ovale. Also, TEE can be avoided in cirrhotic patients with a suspicion of a hepatopulmonary syndrome. These patients often have esophageal varicose veins and often need repetitive gastroscopies. TEE is often performed in stroke patients to detect a possible thromboembolic source in the heart or the great vessels.6,819,20 In patients without an underlying cardiomyopathy, the yield of TEE is low compared with fundamental mode TTE, except when detecting patent foramen ovale. In patients with a normal TTE and in sinus rhythm, the TEE findings of a left atrial thrombus, spontaneous contrast in the left atrium, and complex aortic atheroma are extremely rare.19 In our young stroke patient who did not present with an underlying cardiomyopathy or atrial fibrillation, the only detected thromboembolic risk factor was a patent foramen ovale in 7 of the 21 patients. Therefore, in young patients in sinus rhythm and without a history of cardiac disease, second harmonic mode TTE is a tempting technique to replace TEE and thereby avoid a high workload in the echo laboratory. Using hand-agitated saline solutions, second harmonic mode TTE and TEE are equally sensitive
in detecting right to left shunts in patients undergoing a daily routine TEE. Second harmonic mode TTE is able to differentiate late from early contrast passages. Our observations suggest that the second harmonic mode can be used as an alternative for TEE to calculate patent foramen ovale in divers and young stroke patients without underlying heart disease and without atrial fibrillation. In cirrhotic patients it is able to detect the hepatopulmonary syndrome.
1. Lechat P, Mas JL, Lascault G, Loron PH, Theard M, Klimczac M, Drobinski
G, Thoms D, Grosgogeat Y. Prevalence of patent foramen ovale in patients with stroke. N Engl J Med 1988;318:1148 –1152. 2. de Belder MA, Tourikis L, Leech G, Camm AJ. Risk of patent foramen ovale for thromboembolic events in all age groups. Am J Cardiol 1992;69:1316 –1320. 3. Van Camp G, Schulze D, Cosyns B, Vandenbossche JL. Relation between patent foramen ovale and stroke. Am J Cardiol 1993;71:596 –598. 4. Barzilai B, Waggoner AD, Spessert C, Picus D, Goodenberger D. Twodimensional contrast echocardiography in the detection and follow-up of congenital pulmonary arteriovenous malformations. Am J Cardiol 1991;68:1507– 1510. 5. Vedrinne JM, Duperret S, Bizollon T, Magnin C, Motin J, Trepo C, Ducerf C. Comparison of transesophageal and transthoracic contrast echocardiography for detection of an intrapulmonary shunt in liver disease. Chest 1997;111:1236 – 1240. 6. Pearson AC, Labovitz AJ, Tatineni S, Gomez CR. Superiority of transesophageal echocardiography in detecting cardiac sources of embolism in patients with cerebral ischemia of uncertain etiology. J Am Coll Cardiol 1991;17:66 –72. 7. de Belder MA, Tourikis L, Griffith M. Transesophageal contrast echocardiography and color flow mapping: methods of choice for the detection of shunts at the atrial level? Am Heart J 1992;124:1545–1550. 8. Lee RJ, Bartzokis T, Yeoh TK, Grogin HR, Choi D, Schnittner I. Enhanced detection of intracardiac sources of cerebral emboli by transesophageal echocardiography. Stroke 1991;22:734 –739. 9. Devuyst G, Despland PA, Bogousslavsky J, Jeanrenaud X. Complementarity of contrast transcranial Doppler and contrast transesophageal echocardiography for the detection of patent foramen ovale in stroke patients. Eur Neurol 1997; 38:21–25. 10. Sun JP, Stewart WJ, Hanna J, Thomas JD. Diagnosis of patent foramen ovale by contrast versus color Doppler by transesophageal echocardiography: relation to atrial size. Am Heart J 1996;131:239 –244. 11. Nemec JJ, Marwick TH, Lorig RJ, Davison MB, Chimowitz MI, Litowitz H, Salcedo EE. Comparison of transcranial Doppler ultrasound and transesophageal contrast echocardiography in the detection of interatrial right-to-left shunts. Am J Cardiol 1991;68:1498 –1502. 12. Wilmshurst PT, Byrne JC, Webb-Peploe MM. Relation between interatrial shunts and decompression sickness in divers. Lancet 1989;2:1302–1306. 13. Burns PN, Powers JE, Fritzsch T. Harmonic imaging: a new imaging and Doppler method for contrast enhanced ultrasound (abstr). Radiology 1992;185: 142. 14. Thomas JD, Rubin DN. Tissue harmonic imaging: why does it works? J Am Soc Echocardiogr 1998;11:803– 808. 15. Senior R, Soman P, Khattar, RS, Lahiri A. Improved endocardial visualization with second harmonic imaging compared with fundamental two-dimensional echocardiographic imaging. Am Heart J 1999;138:163–168. 16. Pyles JM, Sawada SG, Feigenbaum H, Segar DS. Enhanced endocardial visualization using harmonic imaging without contrast. Cardiovasc Imag 1998; 10:77– 82. 17. Van Camp G, Cosyns B, Vandenbossche JL. Non-smoke spontaneous contrast in the left atrium intensified by respiratory manoeuvres: a new transoesophageal echocardiographic observation. Br Heart J 1994;72:446 – 451. 18. Ku¨hl HP, Hoffmann R, Merx MW, Franke A, Klo¨tzsch C, Lepper W, Reineke T, Noth J, Hanrath P. Transthoracic echocardiography using second harmonic imaging: diagnostic alternative to transesophageal echocardiography for the detection atral right to left shunt in patients with cerebral embolic events. J Am Coll Cardiol 1999;34:1823–1830. 19. de Belder MA, Lovat LB, Tourikis L, Leech G, Camm AJ. Limitations of transoesophageal echocardiography in patients with focal cerebral ischaemic events. Br Heart J 1992;67:297–303. 20. Leung DY, Black IW, Cranney GB. Selection of patients for transesophageal echocardiography after stroke and systemic embolic events. Role of transthoracic echocardiography. Stroke 1995;26:1820 –1824.
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