Successful Endomyocardial Biopsy Guided by Transthoracic Two-Dimensional Echocardiography A.I. Fiorelli, G.B. Coelho, R.H.B. Santos, J.L. Oliveira Jr, V. Aielo, L. Benvenuti, A.S. Oliveira, M.A.F. Da Silva, P.R. Chizzola, R. Costa, W. Mathias Jr, F. Bacal, E.A. Bocchi, and N.A.G. Stolf ABSTRACT Introduction. Two-dimensional (2-D) echocardiography is an excellent alternative method to perform endomyocardial biopsies (EB) in special situations, mainly when the patient is in a critical state and cannot go to the catheterization laboratory or when there are contraindications to the use of fluoroscopy as in the pregnancy. Objective. This single-center experience analyzed the last 25 years use of an EB technique guided by echocardiography realized at the bedside on critical patients. Methods. From 1985 to 2010, we performed 76 EB guided by 2-D echocardiography on 59 patients, among whom 38 (64.4%) were critically ill with examinations at the bedside; among 10 (16.9%) subjects, the procedure was carried out simultaneously with fluoroscopy for safety’s sake during the learning period. In addition, 8 (13.6%) were unavailable for fluoroscopy, and 3 (5.1%) required a hybrid method due to an intracardiac tumor. Results. The main adverse effects included local pain (n ⫽ 4, 5.6%); difficult out successful puncture due to previous biopsies (n ⫽ 4, 5.6%); local hematoma without major consequences (n ⫽ 3, 4.2%); failed but ultimately successful puncture on the first try due to previous biopsies or (n ⫽ 3, 4.2%); obesity and immediate postoperative period with impossibility to pass the bioptome into the right ventricle; however 2 days later the procedure was repeated successfully by echocardiography (n ⫽ 1, 1.4%). All myocardial specimens displayed suitable size. There were no undesirable extraction effects on the tricuspid valve tissue. In this series, there was no case of death, hemopericardium, or other major complication as a direct consequence of the biopsy. Conclusion. 2-D echocardiography is a special feature to guide EB is mainly in critically ill patients because it can be performed at the bedside without additional risk or disadvantages of fluoroscopy. The hybrid method associating 2-D echocardiography and fluoroscopy allows the procedure in different situations such as intracardiac tumor cases. HE ENDOMYOCARDIAL BIOPSY (EB) technique routinely employs fluoroscopy to guide the bioptome with few adverse effects. In most cases, when there is a high risk to transfer the patient to the catheterization room or a contraindication to the use of fluoroscopy as in pregnancy, an echocardiogram is practical. Sometimes transthoracic or transesophageal echocardiography is useful not only to confirm the position of intracardiac tumors but also to guide the bioptome by providing twoor three-dimensional images.1–3 The greatest advantage of two-dimensional echocardiography to guide an EB is the possibility of accomplish the
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procedure at the bedside and perhaps reduce the risk of perforation by better anatomic definition of the myocardial sampling site. It permits sampling from various ventricular sites, giving preference to the septum.4,5 The aim of the present study was to present our experience at a single center during the last 20 years with the use
From the Heart Institute of Sao Paulo University Medical School, Sao Paulo, Brazil. Address reprint requests to Alfredo I. Fiorelli, Rua Morgado de Mateus 126/81, Sao Paulo/SP, Brazil CEP: 04015-050. E-mail:
[email protected] 0041-1345/–see front matter doi:10.1016/j.transproceed.2010.12.049 225
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Fig 1. (A) Apical four-chamber view obtained by two-dimensional echocardiography. The bioptome (B) is seen (arrow) in the right atrium (RA) and into right ventricle (RV) the tip of bioptome (B) is in the lower third of the interventricular septum. (B) The jaws are opened (large arrows) in the middle of the interventricular septum. This stop-frame image is the exact moment of excision and a little traction is felt at the time of withdrawn the sample.
of two-dimensional echocardiography to guide EB examinations with emphasis on critically ill patients, and calling attention to the advantages of fluoroscopy. METHODS From 1985 to 2010 (25 years), we performed 76 EB guided by two-dimensional echocardiography in 59 patients, including 38 (64.4%) who were critically ill with the exam realized at the bedside; 10 (16.9%), simultaneous with fluoroscopy for safety’s sake during the learning period; 8 (13.6%) unavailable for fluoroscopy; and 3 (5.1%), as a hybrid method due to an intracardiac tumor. The main indicators to EB were in 50 (65.8%) cases, rejection under surveillance, after heart transplantation which were performed in 37 (62.7%) patients; 12 (15.8%) with cardiomyopathy diagnosis before heart transplantation was achieved in 10 (16.9%) patients; 11 (14.5%) with myocarditis diagnosis performed in 9 (15.3%) patients with cardiogenic shock; and 3 (3.9%) with tumor diagnosis into the right chambers in 3 (5.1%) patients. After global echocardiographic evaluation to study cardiac chambers and ejection fraction, the transducer was placed at the subcostal area of the apex for an apical four-chamber view. This position provided better imaging to guide the exam, allowing observation of the movements of the bioptome and inside the heart. It was possible to identify the passage of the bioptome within the superior vena cava, right atrium, and through the tricuspid valve to reach the interventricular septum. An echocardiographic-dense image identified the bioptome and the forceps removing the fragments of the interventricular septum. Contrast saline solution injected into the venous system via the jugular vein improved identification of the cardiac chambers. In each exam, we removed three to six myocardial specimens for histopathologic analysis. We avoided withdrawal of myocardial samples from the free wall of the right ventricle due to the higher risk of perforation. The preferred route of access for percutaneous introduction of the bioptome was the right internal jugular vein using an 8.5-French introducer in 62 (81.6%) biopsies; in other cases, we used the left
internal jugular (n ⫽ 11, 14.5%) or the femoral vein (n ⫽ 3, 3.9%). The catheter guide was useful in special situations such as when the femoral vein was the access route. Patients who needed continuous invasive cardiac monitoring had easy installation of a Swan-Ganz catheter after the biopsy. Hybrid guidance with fluoroscopy and two-dimensional echocardiography was useful to perform bioptome procedures with greater safety during the learning period and in patients with cardiac tumors.
RESULTS
The main adverse effects were pain at the puncture site (n ⫽ 5, 6.6%) patients; puncture difficulty albeit successful due to previous biopsies or obesity (n ⫽ 5, 6.6%), local hematoma without major consequences (n ⫽ 4, 5.3%); chest pain (n ⫽ 3, 3.9%); unsuccessful puncture on the first try due to previous biopsies or obesity (n ⫽ 3, 3.9%) and difficulty due to immediate postoperative status but the successful 2 days later (n ⫽ 1, 1.3%). All myocardial specimens displayed suitable size, and there were not undesirable extraction events in the tricuspid valve or other tissues. There was no case of death, hemopericardium, hemopneumothorax, or other major complications as a direct consequence of the biopsy. The biatrial or bicaval heart transplantation operative technique was not an impediment to notice the EB with two-dimensional echocardiography guidance. Figure 1 shows the details of an EB image guided by two-dimensional echocardiography after heart transplantation using the classic technique. We were successful in visualizing the bioptome and the sampling site in all cases without a cardiovascular complication. No patient needed conversion from echocardiography to fluoroscopy guidance. A patient who was in the second month after heart transplantation was hospi-
TRANSTHORACIC 2-D ECHOCARDIOGRAPHY
talized in the intensive care unit with severe heart failure and suspicion of an acute rejection episode probably due to interruption of immunosuppression. The EB guided by two-dimensional echocardiography was indicated due to the impossibility of transportation. The ejection fraction was below 15%. When the patient was placed in the horizontal decubitus, cardiac arrest occurred during the puncture and the exam was immediately interrupted, however this complication was not related to the procedure. DISCUSSION
Since 1962 when Sakakibara and Konno developed the biopsy catheter, the percutaneous transvenous EB has become a safer, more convenient procedure for rejection surveillance after heart transplantation as well as for histopathologic diagnosis of cardiomyopathies and tumors.6 The EB technique is safe in experienced hands; however, it may lead to several complications, the most serious being right ventricular perforation with cardiac tamponade.2,4,7 Two-dimensional echocardiography has advantages over other imaging modalities, such as equipment mobility, X-ray elimination, and real-time images throughout the procedure. It can be done at the bedside, cardiac catheterization laboratory, cardiovascular intensive care unit, emergency room; indeed, any place that can accommodate a wheeled cart. It provides real-time images showing adequate spatial orientation and anatomic definition. It is helpful in the diagnosis of cardiomyopathy, visualization of intracardiac masses, detection of intracardiac catheters, as well as placement and localization of catheters mainly in the pediatric population.3,8,9 However, the main disadvantage is the necessity for a specialist operator and the greater expense. In 2004, Bedanova et al reported experience with 1262 biopsies collected under echocardiography guidance in 156 patients. Only in 11 patients was there the need for conversion to X-ray guidance and no case of significant tricuspid regurgitation occurred related due to the biopsy.1 After our learning period, the procedure duration time with echocardiographic guidance was comparable to fluoroscopy, namely 10 to 15 minutes. The percutaneous right jugular vein approach was employed more often due to its facility, offering few curves during advance of the bioptome. Both models can be used with catheter or sheath guidance. In patients with artificial cardiac pacing, the puncture is performed on the opposite side. In this series, the surgical technique of heart transplantation did not offer additional difficulties to EB by twodimensional echocardiography, an observation in agreement with other investigations.4,6 Difficulties in the progression of the bioptome occur frequently when there is severe stenosis at the site of the superior vena caval anastomosis.
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Recently the use of real-time transthoracic threedimensional echocardiography in endomyocardial right ventricular biopsies has shown ease and safety both in children and in adults, perhaps with more benefits. Hands experienced to accomplish an EB by fluoroscopy show ease to learn two-dimensional echocardiography as the orientation guide. The view by fluoroscopy in the frontal (or coronal) plane follows the bioptome advance until the transition of the superior or inferior vena cava to the right atrium, and the subsequent entry into the right ventricle across the tricuspid valve. The view by two-dimensional echocardiography is in the transverse plane. The transducer is then located in the subcostal position, and a short-axis plane is visualized, showing the junction between the inferior vena cava and the right atrium. If the femoral vein approach is used, the bioptome can be seen entering the right atrium from the inferior vena cava. When the forceps enters the right atrium, the transducer is rotated to obtain a frontal plane as the subcostal fourchamber view is the more appropriate one (Fig 1). The bioptome advances under echocardiographic control, seen crossing the tricuspid valve and entering the right ventricular cavity. Generally, the primary positioning is not satisfactory, and the catheter must be manipulated using twodimensional echocardiography to position the tip optimally in front of the interventricular septum. The most appalling complication during EB is perforation of the right or left ventricle with cardiac tamponade. It has a high risk of morbidity or death, especially if an inexperienced team is performing the manipulation. Sometimes it has been observed by fluoroscopy that it is difficult to differentiate the apical portion of the septum and the free wall due to dislocation of the tip of the bioptome until the cardiac apex. These situations of greater risk of ventricular perforation occur mainly in dilated cardiomyopathies. EB guidance by two-dimensional echocardiographic may reduce the incidence of complications by providing a better anatomic view of the adequate site where the specimens must be withdrawn, namely the septum and not the right ventricular free wall. In contrast, two-dimensional echocardiography adequately distinguishes the septum from the right ventricular free wall. It also permits patient follow-up after the procedure with immediate detection of complications, such as pericardial effusion or the appearance of a thrombus. Sometimes it is possible to identify the opening and closing of the bioptome jaw (Fig 1). The local pain, hematoma, and other minor complications may be more frequent but are not severe and are generally related to puncture difficulties. This study was not randomized and was performed in a single center with prospective data collection and retrospective analysis. In conclusion, two-dimensional echocardiography is a special method to guide EB mainly in critically ill patients,
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because it can be realized at the bedside and offers no additional risk with advantages over fluoroscopy. In special situations, mainly intracardiac tumor cases, the hybrid combination can be useful. REFERENCES 1. Bedanova H, Necas J, Petrikovits E, et al: Echo-guided endomyocardial biopsy in heart transplant recipients. Transpl Int 17:622, 2004 2. Grande AM, Minzioni G, Martinelli L, et al: Echo-controlled endomyocardial biopsy in orthotopic heart transplantation with bicaval anastomosis. G Ital Cardiol 27:877, 1997 3. Balzer D, Moorhead S, Saffitz JE, et al: Pediatric endomyocardial biopsy performed solely with echocardiographic guidance. J Am Soc Echocardiogr 6:510, 1993 4. Drury JH, Labovitz AJ, Miller LW: Echocardiographic guidance for endomyocardial biopsy. Echocardiography 14:469, 1997
FIORELLI, COELHO, SANTOS ET AL 5. Pytlewski G, Georgeson S, Burke J, et al: Endomyocardial biopsy under transesophageal echocardiographic guidance can be safely performed in the critically ill cardiac transplant recipient. Am J Cardiol 73:1019, 1994 6. Sakakibara S, Konno S: Endomyocardial biopsy. Jpn Heart J 3:537, 1962 7. Fiorelli AI, Coelho GH, Oliveira JL Jr, et al: Endomyocardial biopsy as risk factor in the development of tricuspid insufficiency after heart transplantation. Transplant Proc 41:935, 2009 8. Jackson CE, Gardner RS, Connelly DT: A novel approach for a novel combination: a transseptal biopsy of left atrial mass in recurrent phyllodes tumour. Eur J Echocardiogr 10:171, 2009 9. Abramowitz Y, Hiller N, Perlman G, et al: The diagnosis of primary cardiac lymphoma by right heart catheterization and biopsy using fluoroscopic and transthoracic echocardiographic guidance. Int J Cardiol 118:e39, 2007
