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Ann Thorac Surg 2004;78:862-866
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Transesophageal echocardiography for detecting extrapulmonary thrombi during pulmonary embolectomy

Peter Rosenberger, MDa, Stanton K. Shernan, MDa, Tomislav Mihaljevic, MDa,b, Holger K. Eltzschig, MDa,c,*

a Departments of Anesthesiology, Perioperative and Pain Medicine, Harvard Medical School, Brigham and Women's Hospital, Boston, Massachusetts, USA
b Division of Cardiac Surgery, Harvard Medical School, Brigham and Women's Hospital, Boston, Massachusetts, USA
c Department of Anesthesiology and Intensive Care Medicine, University Hospital, Tübingen, Germany

Accepted for publication February 17, 2004.

* Address reprint requests to Dr Eltzschig, Department of Anesthesiology and Intensive Care Medicine, University Hospital, Hoppe-Seyler Str 3, D-72076 Tübingen, Germany
heltzschig{at}partners.org


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: Pulmonary embolectomy is an evolving surgical procedure for the treatment of severe pulmonary embolism. In addition to removing pulmonary thromboemboli, the achievement of optimal results also requires identification and extraction of intrathoracic, extrapulmonary thromboemboli from the right atrium, right ventricle, and the superior or inferior vena cava. Otherwise, these thromboemboli may become the source of recurrent pulmonary embolism. Intraoperative transesophageal echocardiography is frequently used during pulmonary embolectomy as a guide for the surgeon and a monitor of cardiac performance. However, its utility for detecting concurrent intrathoracic, extrapulmonary thromboemboli has not been thoroughly investigated.

METHODS: The study population included 50 consecutive patients undergoing emergent pulmonary embolectomy. Results from preoperative diagnostic studies including transthoracic echocardiography; ventilation/perfusion scan, pulmonary angiography, and computed tomography were reviewed, along with the intraoperative echocardiographic reports for the presence of intrathoracic extrapulmonary thromboemboli. In addition, the surgical operative notes were consulted to determine the impact of intraoperative transesophageal echocardiography on surgical decision making.

RESULTS: Extrapulmonary intrathoracic thromboemboli were identified preoperatively in 8 patients (16%). Intraoperatively, thromboemboli were identified in 5 additional patients by transesophageal echocardiography, adding to a total of 13 patients with extrapulmonary thrombi (26%). Intraoperative transesophageal echocardiography provided the sole source of evidence that directed surgical management in 10% (5 of 50) of all patients undergoing pulmonary emboletcomy.

CONCLUSIONS: Intraoperative transesophageal echocardiography identified intrathoracic, extrapulmonary thomboemboli in 26% of patients undergoing pulmonary embolectomy, resulting in an alteration of surgical management in 10% of patients. These findings support the critical role of intraoperative echocardiography during pulmonary embolectomy.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Although the management of severe pulmonary embolism can be challenging, the mortality remains high if this disease is not promptly recognized and treated [1]. Compared with thrombolysis, the reduced mortality and incidence of serious complications such as intracranial hemorrhage may favor a surgical therapeutic approach [2]. Pulmonary embolectomy, previously thought to be a treatment of last resort, has recently been associated with very encouraging results for patients with severe pulmonary embolism [3, 4]. As the diagnosis of pulmonary embolism becomes more frequent, promising results from several studies should encourage tertiary centers with the capability of performing pulmonary embolectomy to consider this treatment option earlier within the therapeutic algorithm [5].

Intraoperative transesophageal echocardiography (TEE) is commonly used during pulmonary embolectomy to locate pulmonary embolism, detect residual emboli immediately after the initial procedure, and monitor cardiac performance. In addition, TEE may be used during pulmonary embolectomy to diagnose intrathoracic, extrapulmonary thromboemboli in the inferior vena cava (IVC), the superior vena cava (SVC), the right atrium (RA) or the right ventricle (RV). Although the utility of TEE to detect extrapulmonary thromboemboli has been previously reported, its role as a comprehensive diagnostic tool has not been thoroughly evaluated in a systematic fashion.

During pulmonary embolectomy, the detection of extrapulmonary, intrathoracic thrombi before the institution of cardiopulmonary bypass is critically important. Thrombi in these locations may embolize spontaneously in the perioperative period, or become dislodged during surgical cannulation of the vena cavae or right heart structures. Recurrent thromboemboli are associated with considerable morbidity [6, 7]. For example, free-floating thrombi in the IVC are associated with a mortality rate as high as 40% [8]. Since the diagnosis of extrapulmonary thromboemboli is not always confirmed by preoperative testing, the utility of intraoperative TEE for identifying their presence and location is crucial for the surgical management of patients undergoing pulmonary embolectomy. Therefore, we investigated the utility and impact of intraoperative TEE in identifying extrapulmonary thromboembolism in patients undergoing emergency pulmonary embolectomy.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Subject population
The study population consisted of 50 consecutive patients who underwent pulmonary embolectomy between January 1995 and May 2003 at the Brigham and Women's Hospital, a major tertiary care institution that has a wide referral base for the treatment of pulmonary embolism. Approval for the study was obtained from the Institutional Review Board.

TEE examination
Comprehensive intraoperative TEE examinations were performed using multiplane probes (7 Mhz; Acuson, Mountain View, CA) after the induction of general anesthesia and endotracheal intubation and before the institution of cardiopulmonary bypass. All TEE examinations were performed, videotaped, and interpreted by cardiac anesthesiologists with extensive experience in echocardiography. The most helpful views to evaluate the RA and RV for thromboemboli were the midesophageal four chamber view, the midesophageal right ventricle inflow-outflow view and the transgastric right ventricle inflow view. The RA, IVC, and SVC were evaluated for thromboemboli with the midesophageal bicaval view. Results of the intraoperative TEE examination were provided to the surgical team. Complete results of the intraoperative TEE exam were documented in the patient's medical record. The TEE records were maintained on a computerized database and reviewed in preparation for the present study. Echocardiographic evidence documenting the specific location of any visualized thromboemboli were confirmed by a second cardiac anesthesiologist upon reviewing the TEE videotape in a blinded fashion for the purpose of this study.

Review of surgical operative notes
The detailed surgical operative notes were reviewed to determine the distribution of directly visualized or extracted emboli from different locations within the IVC, SVC, RA, or RV.

Surgical technique
After systemic heparinization, cannulation of the ascending aorta and inferior and superior vena cava was performed. Normothermic cardiopulmonary bypass using vacuum-assisted venous drainage was utilized in all cases. All patients with echocardiographic evidence of extrapulmonary thromboemboli by TEE underwent venous cannulation guided with epicardial echocardiography. Small-diameter cannulas were placed in the areas free of thrombi, and vacuum-assisted venous drainage was used. Pulmonary embolectomy was performed through a Y-shaped incision, which extended from the terminal portion of the pulmonary trunk into proximal aspect of both pulmonary arteries. In all patients with identified thromboemboli in the RA, atriotomy was performed before pulmonary embolectomy to extract the thrombotic material. Extraction of caval thromboemboli was attempted initially through the atriotomy. Alternatively, cold circulatory arrest was used to perform a venotomy and permit extraction of thrombotic material before pulmonary embolectomy.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Subject characteristics
The medical records, intraoperative TEE reports (written and videotape), and surgeon's operative notes of 50 patients (31 men, 19 women), median age 60 years (range, 31 to 86) undergoing emergent pulmonary embolectomy were reviewed. Intensive care unit length of stay (3 days; range, 1 to 52) and hospital length of stay (10 days; range, 1 to 52) varied considerably among patients.

Primary diagnosis of pulmonary embolism
Primary diagnosis of pulmonary embolism was made with a variety of diagnostic techniques (ie, transthoracic echocardiography, ventilation/perfusion scan, pulmonary angiography, or computed tomography) in conjunction with clinical symptoms. Thirteen of 50 patients (26%) were admitted from an outside institution and taken directly to the operating room without further diagnostic evaluation. The presence of extrapulmonary thromboemboli was demonstrated by preoperative diagnostic testing in 8 patients (16%). Intraoperative TEE demonstrated evidence of extrapulmonary thromboemboli in 13 of 50 patients (26%). Thus, intraoperative TEE revealed the previously unappreciated presence of extrapulmonary, intrathoracic thrombi in 5 of 50 patients (10%). There were no discrepancies between the intraoperative TEE written reports and videotaped examinations regarding the diagnosis of extrapulmonary thromboembolism.

Distribution of thromboemboli
Extrapulmonary thromboemboli were discovered during surgery in all 13 previously diagnosed patients. Extrapulmonary thromboemboli were most commonly located in the RA (13 patients). In addition, caval thromboemboli were demonstrated by intraoperative TEE in 6 patients, including 3 previously undiagnosed patients. One patient showed evidence of thromboembolism in the RV (Table 1).


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  		Table 1. Localization of Intrathoracic Extrapulmonary Thrombi Among 50 Patients Undergoing Pulmonary Embolectomy

 
Surgical approach
All 13 patients with RA thromboemboli underwent right atriotomy. Caval thromboemboli were extracted either through right atriotomy (in 2 patients with IVC, and 1 patient with SVC thrombi) or through a venotomy during cold circulatory arrest (in 3 patients with IVC thrombi). The RV thrombus was removed through right atriotomy and extracted through the tricuspid valve.

Mortality rate
The 16% total mortality rate included 2 patients who died intraoperatively. Mortality did not differ among patients with concurrent intrathoracic extrapulmonary thromboemboli (2 of 13 patients) compared with those who presented with only pulmonary embolism (6 of 37).


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Prompt performance of a pulmonary embolectomy shortly after the initial diagnosis of severe pulmonary embolism has been associated with a favorable outcome [3]. Intraoperative TEE is frequently used during this procedure to locate pulmonary embolism and monitor cardiac performance. We hypothesized that intraoperative TEE may also be useful for identifying intrathoracic extrapulmonary thromboemboli. In a series of 50 consecutive patients undergoing pulmonary embolectomy, intrathoracic, extrapulmonary thromboemboli were diagnosed by intraoperative TEE in 26% of the cases. In 5 of 13 (38%) of these patients, a preoperative diagnosis of extrapulmonary emboli had not been made. In all patients, the diagnosis of extrapulmonary thromboemboli prompted surgical evacuation.

Practice guidelines for the perioperative use of TEE proposed by the American Society of Anesthesiologists and Society of Cardiovascular Anesthesiologists classify pulmonary embolectomy as a category II indication, which includes circumstances under which TEE may be useful in improving clinical outcomes, depending on individual circumstances [9, 10]. These guidelines specifically state that intraoperative TEE may be most useful to verify the surgical results by detecting residual thromboemboli within the pulmonary vasculature immediately after the initial pulmonary embolectomy. However, verification of the surgical success may not always be reliable with TEE, as visualization of residual thromboemboli within the pulmonary vasculature may be limited [11, 12]. Alternatively, TEE is a respected and reliable technique for identifying thromboemboli in extrapulmonary locations including both the IVC and SVC (Fig 1) [13]. Moreover, TEE permits optimal visualization of the RA and RV, and is therefore an ideal technique for identifying thrombotic material within these cardiac chambers (Fig 2) [14].



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  		Fig 1. Transgastric basal short axis view of the right ventricle (RV). The RV is occupied by multiple thromboemboli. (RA = right atrium; LV = left ventricle.)

 


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  		Fig 2. Midesophageal bicaval view of the inferior vena cava (IVC). A large embolus is shown (arrow) obstructing hepatic portion of the IVC.

 
During pulmonary embolectomy procedures, extrapulmonary thromboemboli may dislodge during venous cannulation. Furthermore, undiagnosed residual thrombotic material may become a source of recurrent pulmonary embolism postoperatively. Thus, indications for utilizing intraoperative TEE during pulmonary embolectomy should include its utility in diagnosing and locating both the primary pulmonary embolism and concurrent intrathroacic extrapulmonary thromboemboli. Accurately identifying thromboemboli outside the pulmonary arterial circulation can directly impact perioperative decision making in a variety of ways. For example, vascular access procedures may be altered to avoid dislodgment of thromboemboli located in the caval veins or RA during central venous line placement. Moreover, the surgeon's selection of a venous cannulation site and technique for cardiopulmonary bypass may also depend upon the presence of caval and right heart thromboemboli. Transesophageal echocardiography may be particularly useful for guiding venous cannulation in the presence of a mobile thrombus [15]. The incorporation of vacuum-assisted venous drainage into the extracorporeal circuit permits the use of smaller venous cannulas, which can be positioned away from the RA thrombus, thereby minimizing the risk of dislodgment. The identification of concurrent intrathoracic extrapulmonary thromboemboli in patients undergoing pulmonary embolectomy also provides the surgeon with the opportunity to thoroughly evacuate potential retained sources of postoperative recurrent pulmonary embolism. Circulatory arrest may become necessary for a thorough evacuation of thrombotic material from the IVC. That appears critical during pulmonary embolectomy, as thrombotic material within the caval veins can embolize into the pulmonary artery causing recurrent pulmonary embolism or chronic thromboembolic pulmonary hypertension, possibly requiring pulmonary thrombendarterectomy [4, 16]. Thus, intraoperative TEE should be considered a fundamental diagnostic tool in patients undergoing pulmonary embolectomy, unless probe placement is contraindicated or cannot be performed [17]. In these rare circumstances epicardial echocardiography may be a useful alternative for locating both pulmonary embolism and intrathoracic extrapulmonary intrathoracic thromboemboli [18, 19].

The exact incidence of intrathoracic, extrapulmonary thromboemboli in patients with severe pulmonary embolism has not been previously reported. Some case reports have described patients in which TEE identified thromboemboli in the caval veins or within the RA [20]. Chapoutot and colleagues [21] used transthoracic echocardiography in reporting a 7% incidence of intraatrial thrombi in patients with known pulmonary embolism. In contrast, we found a threefold higher incidence of extrapulmonary thromboemboli, which may reflect the superior sensitivity and specificity of TEE compared with transthoracic echocardiography or our higher risk population, which included only those patients who required pulmonary embolectomy [22, 23]. Furthermore, the identification of extrapulmonary thromboemboli by intraoperative TEE was confirmed by surgical exploration, implicating a high positive predictive value. However, we could not confirm the negative predictive value of TEE because surgical evaluation was not pursued in the absence of echocardiographic findings. Thus, it is possible that the incidence of extrapulmonary intrathoracic thromboemboli in patients undergoing pulmonary embolectomy is even higher than estimated in this study. However, this speculation is unlikely considering the high diagnostic accuracy of TEE in evaluating these structures [14, 22, 23].

In conclusion, we have demonstrated that patients with severe pulmonary embolism undergoing pulmonary embolectomy have a relatively high incidence of extrapulmonary thromboemboli. Intraoperative TEE is an excellent, relatively noninvasive technique for evaluating the vena cava and right-side heart structures, and is consequently the most practical diagnostic tool for identifying extrapulmonary intrathoracic thromboemboli in the perioperative period. Thus, the impact of intraoperative TEE on perioperative decision making during pulmonary embolectomy should also include its utility in providing the surgeon with the opportunity to avoid dislodgment of embolic material during venous cannulation and to perform a complete evacuation.


   References
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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