Background
While using echocardiography to guide endomyocardial biopsy (EMB), the authors have identified acute intracardiac thrombus formation related to the procedure, a hitherto unreported complication. The aims of this study were to identify the procedural details and characteristics of patients who developed this complication between June 2008 and April 2009 and to describe their outcomes and management.
Methods
In total, 415 right ventricular biopsies were performed during this period. Of these, 189 were echocardiographically guided, and the medical records of these patients were reviewed retrospectively.
Results
There were eight cases of acute right-sided intracardiac thrombus formation in seven patients (about 4% of the echocardiographically guided group) at the time of biopsy. The indications for EMB were heart transplant surveillance in six patients and suspected cardiac amyloidosis in one patient. Three cases were performed via a transjugular approach and four via a femoral approach. Four patients had histories of prior thromboses, and one patient had a defined clotting diathesis. Management included either immediate thrombus aspiration or postprocedural anticoagulation. There were no overt occurrences of pulmonary thromboembolism.
Conclusions
Acute thrombus formation is a complication of EMB. If this complication is unrecognized, and therefore untreated, pulmonary thromboembolism may result. This may have important clinical implications in patients undergoing routine repeated surveillance EMB after cardiac transplantation. The authors recommend performing transthoracic echocardiography during EMB, particularly in patients with histories of thrombosis, because this group of patients may be at increased risk for procedural thrombosis, and procedural echocardiography permits early recognition and treatment of this complication.
Endomyocardial biopsy (EMB) is currently the technique most often used in the diagnosis of cardiac transplant rejection, and it is the standard method for evaluating infiltrative cardiac lesions, cardiomyopathies, and myocarditis. It is generally considered a safe procedure but is associated with recognized significant complications related to venous cannulation, arrhythmias, and conduction abnormalities as well as inadvertent trauma to cardiac structures such as the tricuspid valve, tricuspid valve apparatus, and right ventricular free wall.
EMB is usually performed under fluoroscopic guidance. However, adjunctive echocardiography is increasingly used because it permits precise positioning of the bioptome, minimizing the risk for complications. In addition, echocardiography facilitates the prompt recognition and treatment of complications if these do occur.
At our institution, we have developed an interventional imaging service that comprises a dedicated core group of sonographers and echocardiographers who provide echocardiographic imaging support in the interventional laboratory. Since June 2008, we have noted a hitherto unreported complication of right ventricular EMB in humans: acute intracardiac thrombus formation. In this study, we describe the characteristics, procedural details, and treatment of seven patients who underwent right ventricular biopsy and developed acute right-sided thrombi during the procedures.
Methods
We identified all patients who underwent EMB at our institution from June 2008 to April 2009 and retrospectively reviewed all the charts of patients undergoing echocardiographically guided endomyocardial biopsies. At our institution, echocardiography is used as a supplemental imaging modality to guide EMB in patients undergoing EMB to diagnose myocardial diseases in patients with ventricular dysfunction or who are undergoing surveillance biopsies who are <3 month after transplantation. Patients who undergo biopsies beyond 3 months after transplantation usually have the procedure performed under fluoroscopic guidance alone, because cardiac perforation is considered unlikely. We recorded the indication for EMB, route of biopsy, number of biopsy specimens taken, and whether the procedure was complicated by thrombus formation. This study was approved by the institutional review board of Mayo Clinic.
EMB
The EMB undertaken in these patients was performed as follows: in the cardiac catheterization laboratory, either the right internal jugular or the right or left femoral vein was prepped and draped. After instillation of a local anesthetic agent, the right or left femoral or right internal jugular vein was entered using the percutaneous technique. An 11-cm sheath (ranging in caliber from 7 to 9 Fr) was placed if an internal jugular vein approach was used. If a transfemoral route was used, an 8-Fr Mullins sheath was inserted into the femoral vein. Next, a bioptome (ranging in caliber from 6 to 9 Fr; Cordis Corporation, Miami Lakes, FL, or Scholten Surgical Instruments, Inc, Lodi, CA), was inserted into the sheath and advanced to the right ventricle. Once the position of the bioptome tip was in an ideal location, guided by transthoracic echocardiography (see below), an EMB was obtained. After each biopsy, the bioptome was removed from the heart and reinserted until a satisfactory number of specimens had been obtained. The venous sheaths were not routinely flushed during the procedure. After the last biopsy specimen had been obtained, the bioptome and sheath were removed and pressure was applied to the puncture site until hemostasis was achieved. The procedure was performed under fluoroscopic and echocardiographic guidance.
Echocardiographic Imaging
Echocardiographic imaging was performed using standard transthoracic machines using standard imaging probes (iE33 machine with an S5-1 probe, Philips Medical Systems, Andover, MA; and Vivid I laptop machine using a GE 3S-rs probe, GE Healthcare, Milwaukee, WI). Harmonic imaging was routinely used to optimize image quality. The patient was imaged in the cardiac catheterization laboratory while lying supine on the procedure table. Generally, the patient was already prepped and draped before imaging. No specific echocardiographic views were obtained. Generally, scanning was performed left-handed from the left side of the bed, and apical or para-apical views were obtained. Attention was paid to obtain the best longitudinal-axis images of the right atrium and right ventricle, tricuspid valve, and tricuspid apparatus as well as ensuring that the bioptome tip could be visualized in the right ventricle before biopsy. Baseline imaging was performed immediately before the procedure, and then imaging was repeated during bioptome insertion, positioning, and biopsy and immediately on withdrawal of the bioptome to evaluate for tricuspid regurgitation and assess for a pericardial effusion. This imaging sequence was repeated for each biopsy attempt until the conclusion of the case. Occasionally, because of poor apical window image quality, a subcostal window was used.
Results
There were 415 right ventricular biopsies performed in 212 patients at the Mayo Clinic from June 2008 to April 2009. Of these biopsy procedures, 189 were echocardiographically guided (undertaken in 90 patients). One hundred thirty-five of these biopsies (71.4%) were performed for transplant surveillance, 40 (21.1%) for evaluation of the etiology of left ventricular dysfunction, and 14 (7.4%) to rule out cardiac amyloidosis. The route of EMB was most frequently from the right internal jugular vein (77.3%). Access via the right femoral vein was used in 21.1% of cases and access via the left femoral vein in 1.6%. Most commonly, five biopsy specimens were obtained per procedure (76.2%), with a range of zero to eight biopsy specimens.
In eight of 189 of the echocardiographically guided procedures (4%), acute thrombi were identified at the time of the biopsy, usually toward the end of the procedure, in seven patients (one patient experienced acute thrombus formation on two separate occasions; Figure 1 ). Although the majority of procedures were performed from a right internal jugular approach, acute thrombus formation occurred in only three of 143 of these procedures (2%). Thrombus occurred most frequently when a right femoral vein access site was used (five of 35 procedures [12.5%]). The left femoral vein was used in only three procedures, and no thrombus developed in any of these cases. There was no clear association between number of biopsy specimens obtained and risk for thrombus. Of the eight procedures in which thrombi were detected, five biopsies were performed in three procedures, three biopsies in two procedures, and one, six, and seven biopsies in one procedure each.
Clinical and Echocardiographic Characteristics of Patients Who Developed Thrombi
The mean age of the seven patients who developed thrombi during EMB was 48 ± 10 years. Three were men. The indication for the biopsy was surveillance of heart transplantation in six patients (representing 5.2% of echocardiographically guided transplant surveillance EMB procedures) and evaluation for suspected cardiac amyloidosis in one patient (7.1% of echocardiographically guided EMB procedures to detect cardiac amyloidosis). Histology ultimately confirmed a diagnosis of cardiac amyloidosis in this patient.
Four patients had histories of thrombosis, and one patient had a defined clotting diathesis. Table 1 summarizes the general characteristics and pertinent medical histories of all seven patients in whom thrombi were identified, while Table 2 summarizes the clinical features of the heart transplantation patients in particular. The echocardiographic characteristics of these patients are summarized in Table 3 and Videos 1-4 ( view video clips online).
| Patient | Gender | Age (years) | EMB indication | Prior thrombosis | Comorbidities |
|---|---|---|---|---|---|
| 1 | Male | 52 | HTX | Left internal jugular DVT | HL, HT, ICD before HTX |
| 2 | Female | 50 | HTX | Left cephalic vein thrombosis and right internal jugular DVT | Radiation and chemotherapy for breast cancer, ICD before HTX |
| 3 | Female | 48 | HTX | Right and left subclavian vein DVT, left internal jugular vein DVT, pulmonary embolism | Asthma, steroid-induced DM |
| 4 | Male | 46 | HTX | VAD cannula thrombosis, right internal jugular vein thrombosis, TIA | HT, HL, CRT-D before HTX |
| 5 | Male | 62 | HTX | No | Multiple sclerosis, HT, paralyzed left hemidiaphragm, LVAD infection before HTX |
| 6 | Female | 50 | Amyloidosis | Stroke | PPM, colitis, hepatitis B |
| 7 | Female | 29 | HTX | No | Rheumatoid arthritis, thrombocytopenia |
| Patient | HTX indication | LVAD before HTX | Complications after HTX | Immunosuppressive medications at time of EMB | Time interval between HTX and EMB |
|---|---|---|---|---|---|
| 1 | Ischemic cardiomyopathy | No | Graft dysfunction, bronchial bleeding, RV dysfunction | Cyclosporine, MM, prednisone | 7 weeks |
| 2 | Restrictive cardiomyopathy secondary to doxorubicin and radiation | Yes | No | Cyclosporine, MM, prednisone | 6 months |
| 3 | Eosinophilic myocarditis | Yes | Pulmonary bleeding, loculated pleural effusion, bilateral upper DVT | Cyclosporine, MM, prednisone | 3 weeks |
| 4 | Idiopathic dilated cardiomyopathy | Yes | No | Cyclosporine, MM, prednisone | 3 months |
| 5 | Ischemic cardiomyopathy | Yes | Colonic perforation | Cyclosporine, MM, prednisone | 6 months |
| 7 | Idiopathic pulmonary hypertension | No | Pleural and mediastinal bleeding, pneumonia and respiratory failure | Cyclosporine, MM, prednisone | 3 months |
| Patient | RV size | RV function | TV morphology | TR velocity before biopsy (m/sec) | TR severity | LV size (diastolic/systolic dimension in mm) | LV EF (%) |
|---|---|---|---|---|---|---|---|
| 1 | Moderate increase | Mild decrease | Intact | 2.8 | Moderate | 45/32 | 60 |
| 2 | N | N | Intact | 2.5 | Mild | 45/30 | 66 |
| 3 | N | N | Intact | 3.1 | Mild | 43/24 | 72 |
| 4 | N | N | Flail segment | 2.8 | Severe | 41/28 | 58 |
| 5 | N | N | Intact | Unable to detect | Trivial | 48/39 | 37 |
| 6 | N | N | Intact | 3.1 | Severe | 56/37 | 65 |
| 7 | Mild increase | N | Intact | 2.4 | Trivial | 47/33 | 60 |
Regarding the procedural details, three cases were performed via a transjugular approach using an 11-cm sheath ranging in caliber from 7 to 9 Fr, inserted into the right internal jugular vein, and four were performed via a femoral approach using an 8-Fr Mullins sheath inserted into the right femoral vein. A bioptome ranging in caliber from 6 to 9 Fr, manufactured by Cordis Corporation ( n = 4) or Scholten Surgical Instruments ( n = 3), was used in these cases. See Table 4 for the characteristics of the EMB in each patient. In one patient (patient 4), unique thrombus formation occurred on two successive EMB attempts, 2 weeks apart. In this patient, interval echocardiography confirmed resolution of the index thrombus after treatment with systemic anticoagulation. However, another thrombus formed during subsequent EMB despite continuous flushing and frequent aspiration of the Mullins sheath throughout the procedure. Management included either immediate thrombus aspiration or systemic anticoagulation post procedure. There were no overt occurrences of pulmonary thromboembolism. Table 5 summarizes the specific thrombus location and individual patient management in all eight cases.
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