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Ann Thorac Surg 2009;88:1556-1565. doi:10.1016/j.athoracsur.2009.06.011
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Surgical Lung Resection for Severe Hemoptysis

Claire Andréjak, MDa, Antoine Parrot, MDa, Bernard Bazelly, MDb, Pierre Yves Ancel, MDc, Michel Djibré, MDa, Antoine Khalil, MDd, Dominique Grunenwald, MDb, Muriel Fartoukh, MDa,*

a Respiratory, Tenon Hospital, Assistance Publique - Hôpitaux de Paris and Pierre et Marie Curie University and INSERM U 149, Paris, France
b Critical Care, Tenon Hospital, Assistance Publique - Hôpitaux de Paris and Pierre et Marie Curie University and INSERM U 149, Paris, France
c Thoracic Surgery, Tenon Hospital, Assistance Publique - Hôpitaux de Paris and Pierre et Marie Curie University and INSERM U 149, Paris, France
d Radiology Department, Tenon Hospital, Assistance Publique - Hôpitaux de Paris and Pierre et Marie Curie University and INSERM U 149, Paris, France

Accepted for publication June 4, 2009.

* Address correspondence to Dr Fartoukh, Hôpital Tenon, Assistance Publique, Hôpitaux de Paris, 04 rue de la Chine, Paris, 75020, France (Email: muriel.fartoukh{at}tnn.aphp.fr).


GENERAL THORACIC SURGERY: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: The role of surgical lung resection in the management of severe hemoptysis has evolved after advances in interventional radiology. We sought to describe the indications for surgical lung resection in such patients and to identify predictive factors of postoperative complications.

Methods: This study is a retrospective analysis (May 1995 to July 2006) of consecutive patients referred to the intensive care unit of a tertiary hospital for severe hemoptysis who underwent surgical lung resection.

Results: Among 813 patients referred for severe hemoptysis, 111 underwent surgical lung resection. Interventional radiology had been first attempted in 87 patients (78%); 68 underwent surgery because of a failed procedure (n = 28) or bleeding persistence or recurrence within 72 hours despite a completed procedure (n = 40); 19 patients underwent surgery after bleeding control. The remaining 24 patients (22%) were directly referred to the surgeon (5 for emergency surgery). Overall, surgery was performed in emergency (n = 48), scheduled after bleeding control (n = 48), or planned after discharge (n = 15). The main indications for surgery were mycetoma, cancer, bronchiectasis, and active tuberculosis. Surgery for mycetoma (odds ratio, 9.4; 95% confidence interval, 2.8 to 32), emergency surgery (odds ratio, 5.3; 95% confidence interval, 1.8 to 16), and pneumonectomy (odds ratio, 4.7; 95% confidence interval, 1.2 to 18) independently predicted complications. Fifteen patients died in the intensive care unit, of whom 14 underwent emergency surgery. Chronic alcoholism (odds ratio, 4.6; 95% confidence interval, 1.1 to 19), the need for mechanical ventilation or vasoactive drugs on admission (odds ratio, 8.2; 95% confidence interval, 1.9 to 35), and blood transfusion before surgery (odds ratio, 8; 95% confidence interval, 1.5 to 42) predicted mortality.

Conclusions: Attempting at controlling bleeding with first-line nonsurgical approaches appears necessary to optimize the operative conditions and improve outcome of patients with severe hemoptysis.

Severe hemoptysis (SH) is a life-threatening condition associated with a high mortality rate in the absence of adequate treatment. Until two decades ago, surgical lung resection was considered as the treatment of choice for SH in patients with adequate pulmonary function, with the only alternative being general supportive care [1, 2]. Surgical lung resection for SH was also reputed to be associated with high morbidity and mortality, especially when performed during active bleeding [3–6]. The management of SH has largely evolved since the first reports of successful bronchial artery embolization (BAE) [7], now considered as first-line therapy [8, 9]. Furthermore, more advanced and promising interventional radiology procedures have been recently developed such as pulmonary angiography with vasoocclusion [10]. However, no controlled study has compared the medical (including interventional radiology) versus the surgical approach in the initial management of SH. Even if BAE, and more generally interventional radiology, has become widely used, a subset of patients with SH still requires surgical lung resection at the early stage of their management.

In this study, we analyze a series of consecutive patients with SH referred to a single intensive care unit (ICU) with an affiliated step-down unit (respectively, 10 and 6 beds) who underwent surgical lung resection. These patients were selected from a large cohort of 813 patients referred to our unit for SH. Our aims were (1) to identify factors associated with surgery among patients with SH; (2) to describe the clinical epidemiology of patients referred to surgery and the conditions in which surgery was performed; and (3) to identify factors associated with postoperative complications and ICU mortality, accounting for whether bleeding was controlled or not at time of surgery. The study was conducted in accordance with French law, which does not require approval of an institutional review board or individual patients' consent for such retrospective analysis of medical records.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patients
The study was conducted during an 11-year period (May 1995 to July 2006) at Tenon Hospital, a tertiary university hospital and referral center for hemoptysis in Paris, France. All consecutive patients admitted to our institution with SH who underwent surgical lung resection were eligible. Patients with hemoptysis who underwent a diagnostic open lung biopsy were excluded. For each patient, baseline demographics, comorbid conditions, initial clinical presentation and vital signs, cause of hemoptysis, management, indications and conditions of surgery, ICU and hospital lengths of stay, and vital status at discharge were recorded.

Definitions
Severity of hemoptysis
One of the following conditions defined SH: (1) a cumulative amount of bleeding on admission of at least 200 mL within the preceding 72 hours in case of normal or nearly normal lung function, (2) acute respiratory failure, (3) use of intravenous vasoconstrictive agent (terlipressin), and (4) need for blood transfusions. The cumulative amount of bleeding was assessed from the onset of bleeding until the first hours of admission to our unit using the following scale: a spoonful (5 mL), a small filled glass (100 mL), and a large filled glass (200 mL). Acute respiratory failure was defined as room air oxygen saturation less than 90% or a respiratory rate greater than 25 breaths/min, and the requirement for high-flow oxygen or mechanical ventilation.

Cause of hemoptysis
The cause of hemoptysis was diagnosed on the combination of detailed medical history, physical examination, chest roentgenograph, fiberoptic bronchoscopy, computed tomography scan, microbiologic results if performed, and pathologic examination of lung tissue resected.

Management
The main objective of the initial management was to control the bleeding to prevent asphyxiation. The patients received general supportive care in a uniform way, as described elsewhere [11]. The severity of bleeding was assessed on the need for administration of local or systemic vasopressors (terlipressin), mechanical ventilation, or blood transfusions or vasoactive drugs (epinephrine, norepinephrine) to control hypotension, before referral or within the first 24 hours of ICU admission. Intrabronchial procedures used in an attempt to control the bleeding combined the bronchoscopic topical techniques (blood aspiration, local instillation of cold saline lavage and of vasopressors if needed), the bronchoscopic placement of a balloon, the administration of intravenous terlipressin, and the use of a double-lumen endotracheal tube or a selective intubation.

A bronchial arteriography was first attempted for BAE in combination with general supportive care. In case of an unstable catheter or dangerous collaterals, a superselective catheterization was performed using a microcatheter, as recommended [12]. A pulmonary angiography, if possible associated with pulmonary vasoocclusion, was performed alone in patients with hemoptysis suspected of a pulmonary arterial mechanism, or in association with BAE in patients with persistent or recurrent bleeding. Failure of attempted bronchial arteriography refers to the persistence of bleeding in the following situations: no systemic hypervascularization, inability to cannulate the vessel, or instability of the catheter tip despite superselective catheterization. Failure of the attempted pulmonary angiography refers to the lack of demonstration of a pulmonary arterial source for hemoptysis. Failure of completed bronchial arteriography (or pulmonary angiography) refers to the persistence or the recurrence of bleeding despite embolization (or vasoocclusion).

The timing of surgery was defined as emergency surgery, scheduled, or planned. Emergency surgical resection was performed during active and uncontrolled bleeding. When performed after control of bleeding, surgery was either scheduled during the same hospitalization, or secondarily planned (within 6 months of discharge), because of an expected high risk of recurrence of bleeding.

Outcome
Intraoperative complications included the following events occurring during surgery: acute hemorrhagic anemia (defined as the need for blood products transfusion), shock (defined as the need for intravenous infusion of vasopressors such as epinephrine or norepinephrine), and death.

Postoperative complications were defined as complications occurring 24 hours or more after surgery and included (1) the need for mechanical ventilation; (2) the need for blood products transfusion; (3) the need for infusion of vasopressor drugs (epinephrine, norepinephrine) to maintain hemodynamic stability; (4) the occurrence of a bronchopleural fistula, a pneumonia or any extrapulmonary hospital-acquired infection; and (5) death.

Intensive care unit and hospital lengths of stay and vital status at discharge were recorded. The follow-up was conducted during a visit in our institution or by a telephone interview after discharge.

Statistical Analysis
Our study first aimed at analyzing the factors associated with performing surgical lung resection and describing the clinical epidemiology of patients with SH who underwent surgery. The patients' demographics and clinical variables were analyzed, using usual descriptive statistics. Results are expressed as mean ± standard deviation (range), unless otherwise stated. The Mann-Whitney U test was used for quantitative variables and the {chi}2 test or Fisher's exact test for nominal variables. A probability value less than 0.05 was considered statistically significant.

Second, we identified predictive factors of postoperative complications and of ICU mortality by performing multivariate analyses using a stepwise backward logistic regression. The number of events per variable entered in the final multivariate model averaged a ratio of 10 to avoid overfitting, as recommended [13]. The simplified acute physiology score (SAPS II) was not entered in both multivariate analyses, because it encompassed numerous variables used to define organ failures that overlapped with other variables considered in the models.

Univariate analysis first assessed the association between each variable and postoperative complications. Variables selected by univariate analysis (p < 0.2) and those considered clinically relevant (tobacco exposure, mechanical ventilation or vasoactive drugs on admission, blood transfusion, cause of hemoptysis, conditions of surgery, and surgical procedure) were entered in a logistic regression model to identify the predictors of postoperative complications. For the analysis of ICU mortality, clinically relevant variables (chronic alcoholism, mechanical ventilation or vasoactive drugs on admission, and blood transfusion) selected by univariate analysis were entered in a logistic regression model to identify predictors of ICU mortality. Emergency surgery was not entered in this model, because most patients (n = 14 of 15; 93%) who died in the ICU had undergone emergency surgical resection. The results are reported using odds ratio (OR) and corresponding 95% confidence intervals (CI). All statistical analyses were performed on a personal computer using the Statview software (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
During the 11-year study period, 813 consecutive patients were referred to our unit for SH, of whom 116 (14%) underwent a surgical lung resection. Five patients were excluded from the analysis (diagnostic surgical lung biopsy, n = 2; surgery planned 6 months after the initial episode of hemoptysis, n = 2; and surgery performed at another center, n = 1). Overall, 111 patients undergoing surgical resection for SH in our center were analyzed. Some of these patients have been described elsewhere [11, 14, 15]. Twenty-nine medical patients had missing data and were excluded. The characteristics of patients managed with general supportive care and interventional radiology only (n = 668) or undergoing surgery (n = 111) are shown in Table 1. Variables associated with performing surgery were related to the magnitude and consequences of bleeding (volume of bleeding, mechanical ventilation, or shock), the noncontrol of bleeding using general supportive care and interventional radiology, or an expected high risk of bleeding recurrence related to the cause or the mechanism of hemoptysis.


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  		Table 1 Characteristics of 779 Patients With Hemoptysis, Contrasting Medical and Surgical Patients
 
Patients undergoing surgery (82 males) were aged 50 ± 14 years. Most of them were referred from another hospital (n = 74; 67%). The mean time between bleeding onset and referral to our unit was 3 ± 5 days (median time, 1 day; Table 2). Forty-nine patients (44%) received intravenous terlipressin before referral (n = 36), or during the first 24 hours of admission (n = 13). Sixty-one patients (55%) presented with acute respiratory failure, and 15 required mechanical ventilation within the first 24 hours. Blood transfusions were administered to 21 patients (19%) during the first 24 hours and overall to 40 patients (36%) before surgery. Vasoactive drugs (epinephrine, norepinephrine) were administered to 14 patients (13%) within the first 24 hours of ICU admission. Bronchoscopic techniques, combining blood aspiration and local instillation of cold saline solution, were performed in 57 patients (51%). Terlipressin or adrenaline was bronchoscopically delivered in 47 patients (42%), and a balloon was placed in 6 (12%). The main indications for surgery were mycetoma (25%), cancer (22%), bronchiectasis (19%), and tuberculosis (7%) (Table 1).


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  		Table 2 Clinical Characteristics of the Surgical Population a
 
Twenty-four patients (22%) were referred directly to the surgeon for lung resection, ie, without first-line attempt to undergo interventional radiology. The indications for direct surgical referral included an expected technically hazardous procedure of BAE (n = 2), a recent history of massive bleeding treated with a completed procedure of interventional radiology (n = 5), involvement of the proximal region of a pulmonary artery (n = 2), the associated need for a pathologic examination for diagnostic purposes (n = 10), an origin for the SH requiring a definitive surgical treatment (mycetoma, n = 5). In these 24 patients, surgery was performed in emergency (n = 5), scheduled (n = 11), or was secondarily planned (n = 8).

A first-line interventional radiology procedure was attempted in the remaining 87 patients (78%), including a bronchial arteriography in 83 patients (completed with embolization in 57) and a pulmonary angiography in 4 (completed with vasoocclusion in 2) (Table 3). Nineteen of these patients had initial control of bleeding and were secondarily referred to surgery, mostly because of a high-risk origin of the SH. Technical failure of interventional radiology occurred in 28 patients. Hemoptysis persisted or recurred during hospitalization in the remaining 40. Overall, 43 of these 68 patients who failed first-line interventional radiology were operated on in emergency (Fig 1).


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  		Table 3 Details of Circumstances Leading to Surgical Lung Resection in 111 Patients
 

Figure 1
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  		Fig 1. Performance of first-line interventional radiology in patients with severe hemoptysis (SH) undergoing surgical lung resection. Technical failure of interventional radiology was recorded for 28 patients (32%), including 26 of the 83 patients who underwent a bronchial arteriography and 2 of the 4 patients who underwent a pulmonary angiography. Bronchial arteriography was eventually completed with embolization in 57 of 83 patients (69%), leading to immediate bleeding control in one third of them (n = 17; 30%), whereas hemoptysis persisted or recurred during hospitalization in the remainder (n = 40; 70%). Pulmonary vasoocclusion was completed in 2 of 4 patients resulting in immediate bleeding control. Finally, 43 of the 68 patients who failed first-line interventional radiology were operated on in emergency.

 
Altogether, surgical resection was performed in emergency during active bleeding in 48 patients (43%) within 5 ± 6 days of referral, or was performed during the same hospitalization after control of bleeding (ie, scheduled) within a mean of 8.5 ± 7 days in 48 patients (43%). In the remaining 15 patients (14%), surgical resection was secondarily planned and performed after a mean of 61 ± 49 days (Table 3). Altogether, the surgical resection involved one lobe in 78 patients (72%), one lung in 21 (19%), and a segmental resection was performed in 9 patients (8%).

Surgery was uneventful in 66 patients (61%). Intraoperative complications occurred in 43 patients, including acute hemorrhagic anemia, shock, and cardiac arrest in, respectively, 37 (34%), 24 (22%), and 4 patients (4%) (Table 4); 3 deaths occurred during emergency surgery. Excluding those 3 patients, 49 patients (46%) had postoperative complications. Surgery for mycetoma (OR, 9.4; 95% CI, 2.8 to 32), emergency surgical resection (OR, 5.3; 95% CI, 1.8 to 16), and pneumonectomy (OR, 4.7; 95% CI, 1.2 to 18) were independent predictors of post-operative complications (Table 5).


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  		Table 4 Outcome of 111 Patients Undergoing Lung Resection for Severe Hemoptysis a
 

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  		Table 5 Univariate and Multivariate Analyses of Variables Associated With Postoperative Complications in 111 Patients Undergoing Surgical Lung Resection a
 
The lengths of ICU and hospital stay were respectively 15 ± 18 days (range, 0 to 95 days) and 25 ± 22 days (range, 0 to 142 days). The overall ICU and hospital mortality rates were 13.5% (n = 15) and 17% (n = 19), respectively; corresponding figures for emergency surgery were 29% and 35% (Table 4); all but 1 of the 15 patients who died in the ICU and 17 of the 19 patients who died in the hospital underwent emergency surgery during active bleeding. In multivariate analysis, chronic alcoholism (OR, 4.6; 95% CI, 1.1 to 19), the need for mechanical ventilation or for vasoactive drugs on admission (OR, 8.2; 95% CI, 1.9 to 35), and blood transfusion before surgery (OR, 8; 95% CI, 1.5 to 42) were independently predictive of ICU mortality (Table 6).


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  		Table 6 Univariate and Multivariate Analyses of Variables Associated With Intensive Care Unit Mortality in 111 Patients Undergoing Surgical Lung Resection a
 
At short-term follow-up (1 month), hemoptysis was successfully controlled in all patients discharged from hospital. Hemoptysis recurred in 5 patients (4.5%) with mycetoma (n = 3), bronchiectasis (n = 1), or cancer (n = 1), after a mean (median) follow-up duration of 16 (5.8) months.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
We investigated the role of surgery in the management of a large series of patients referred for SH in the era of interventional radiology. Surgery was indicated in about 14% of patients, with emergency surgery representing nearly half of the procedures, mostly after failed attempt or unsuccessful interventional radiology. A similar proportion underwent scheduled surgery during the same hospital admission, after bleeding was controlled using general supportive care alone or combined with interventional radiology; finally, a small proportion (15%) underwent secondarily planned surgery, mostly because of a cause or mechanism considered at high risk of recurrence of severe bleeding. The main causes of hemoptysis were mycetoma, cancer, bronchiectasis, and active tuberculosis. Postoperative complications were related to the magnitude of hemoptysis (blood products transfusion), the conditions (emergency) and type (pneumonectomy) of surgery, and the cause of hemoptysis (mycetoma). Chronic alcoholism and the need for mechanical ventilation or hemodynamic support with vasoactive drugs on admission and for blood transfusion were independently associated with ICU mortality.

Criteria defining SH include the amount as well as the consequences of blood loss, the underlying pulmonary function, and the cause of hemoptysis [16, 17]. In our series of surgical patients, the mean cumulated volume averaged 225 mL on ICU admission. Half of the patients had acute respiratory failure on admission, and one third received blood product transfusions before surgery. The causes of SH have progressively shifted from infectious causes to chronic inflammatory lung diseases, especially in industrialized countries, with bronchiectasis, cancer, tuberculosis, and mycetoma accounting for most causes [11, 17–19], as in our series.

The priorities in treating SH are first to provide general supportive care, ie, maintain free airways, optimize oxygenation, and stabilize hemodynamic condition, then to localize the site and to diagnose the cause and the mechanism(s) of bleeding, and lastly to administer definitive treatments to prevent massive or fatal bleeding recurrence [16, 20, 21].

Historically, surgical lung resection was considered as the only procedure available to improve survival in life-threatening hemoptysis [2]. The "natural history" of massive hemoptysis was indeed associated with a catastrophic outcome in historical series, reporting a 78% to 85% mortality rate in patients eligible for surgery but in whom surgery was not performed [4, 6], whereas mortality rate decreased to less than 30% in patients undergoing surgery [4]. Therefore, most patients with SH underwent surgery, which was considered as the standard of care in the 1980s [1]. During the past two decades, the role of surgery has been progressively reduced, owing to improvements in general supportive care [16, 20–25] and major advances in interventional radiology [10, 26–28]. When feasible, BAE is associated with an immediate control of bleeding in 80% to 100% of cases, with a bleeding recurrence rate averaging 5% to 20%, including in our own experience [11, 12, 17, 19].

In the present series of 111 patients undergoing surgery, an interventional radiology procedure was attempted in 87 of the patients (78%) and completed in 68%; however, an immediate control of bleeding was obtained in only one third of these. Moreover, bleeding recurred frequently. In our experience, the main indications for surgery were related to the magnitude of bleeding and uncontrolled bleeding after interventional radiology, or the expected high risk of bleeding recurrence owing to the cause or mechanism of bleeding. The poor performance of BAE in this subset of patients referred to surgery might be attributable in part to the liberal use of intravenous terlipressin, and to the large proportion of patients with mycetoma in this subset, a common cause of BAE failure and recurrent bleeding [11, 29, 30]. Additionally, microcatheters were not routinely used in our center until the early 2000s.

Surgical lung resection within the context of hemoptysis is traditionally associated with high morbidity and mortality. The difficult conditions of surgical resection when performed during massive and active bleeding and pneumonectomy are well-recognized factors increasing the risk of postoperative complications and mortality [3–6]. Consistently, nearly one half of our patients had postoperative complications, especially those with the more severe blood loss, having mycetoma, and undergoing emergency surgery and pneumonectomy. In the series of 43 patients reported by Jougon and colleagues [31], the overall mortality rate was 19% and rose to 27% when surgical resection was performed during active bleeding, as compared with no death when surgery was secondarily performed after control of bleeding. Similarly, in our series, the ICU mortality was 13.5% and the overall hospital mortality, 17.1%; however, hospital mortality was 35% in patients operated on during active bleeding versus 4% in those operated on later, after control of bleeding.

Chronic alcoholism, the need for mechanical ventilation or for vasoactive drugs on admission, and blood transfusion before surgery were independently predictive of ICU mortality. Whereas smoking is well known to be associated with operative morbidity and mortality, the adverse effect of chronic alcoholism on the outcome of lung resection has rarely been reported. In a retrospective series of 107 patients undergoing surgical resection for lung cancer, postoperative mortality significantly increased among chronic alcohol users [32]. In our series, mortality was also related to the need for mechanical ventilation or hemodynamic support with vasoactive drugs and blood transfusion before surgery, again reflecting massive or uncontrolled bleeding and the emergent conditions of surgery, similarly to other series [31].

Our results raise the issue of the safety of performing emergency surgical lung resection in patients with SH and persistent bleeding, and suggest that every attempt should be made to control bleeding before surgery. Multidetector computed tomography angiography should be first performed to identify the cause and mechanism of hemoptysis [10, 27, 28]. Bronchial artery embolization should be considered as the first-line procedure for active bleeding originating from the systemic bronchial vessels, and often allows postponement of surgery [31]. Conversely, in the rare cases of hemoptysis originating from the pulmonary vessels, pulmonary artery occlusion or endovascular stent graft should be attempted first [10]. In case of failure of endovascular treatment or in selected high-risk patients (chronic alcoholism, initial acute respiratory failure, or hypotension) with persistent hemoptysis, other approaches such as the use of recombinant factor VII [22] or bronchial topical treatment [25, 33] should be considered to control bleeding before surgery. Once hemoptysis has been controlled, surgical lung resection remains the treatment of choice to prevent recurrences from cavitary lesions, atrophic lung segments as a result of chronic infection, and nonsystemic hypervascularization on BAE [34]. Failure of the above approaches requires emergency surgery for lung resection. Other surgical modalities (physiologic lung exclusion) have been described in cases in which lung resection is technically hazardous or difficult. Dhaliwal and associates [35] reported the efficacy and safety of the surgical ligation of the bronchus and pulmonary artery of the involved lobe or lung in a series of 20 patients with hemoptysis related to tuberculosis. There were no deaths, and hemoptysis did not recur.

The limitations of our study are related to its retrospective nature and to the fact that it was conducted in a referral center with an extensive experience of hemoptysis. Nevertheless, our large series allows us to more clearly delineate the current indications for surgery in patients with SH and to identify preoperative factors associated with a poor outcome.

In sum, although emergency surgical lung resection is no longer the initial treatment for SH, some patients will still need surgery. Attempting at controlling hemoptysis with first-line nonsurgical approaches appears necessary, however, to optimize the operative conditions and improve morbidity and mortality.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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Invited Commentary
Song Wan and Anthony P.C. Yim
Ann. Thorac. Surg. 2009 88: 1565. [Extract] [Full Text] [PDF]



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S. Wan and A. P.C. Yim
Invited commentary.
Ann. Thorac. Surg., November 1, 2009; 88(5): 1565 - 1565.
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