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Ann Thorac Surg 2004;78:1224-1228
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Short- and Long-Term Outcomes after Large Pulmonary Resection for Germ Cell Tumors After Bleomycin-Combination Chemotherapy

Rafael S. Andrade, MDa, Kenneth A. Kesler, MDa, Jamison L. Wilson, MSa, Jo Ann Brooks, DNSa,*, Brett D. Reichwage, MSa, Karen M. Rieger, MDa, Lawrence H. Einhorn, MDb, John W. Brown, MDa

a Department of Surgery, Thoracic Division, Indiana University School of Medicine, Indianapolis, Indiana, USA
b Department of Medicine, Oncology Division, Indiana University School of Medicine, Indianapolis, Indiana, USA

Accepted for publication March 30, 2004.

* Address reprint requests to Dr Kesler, Indiana University School of Medicine, Department of Surgery, Thoracic Division, 545 Barnhill Dr, EH 215, Indianapolis, IN, USA 46202
kkesler{at}iupui.edu


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Treatment of nonseminomatous germ cell tumors frequently requires bleomycin-combination chemotherapy followed by resection of residual disease. Bleomycin administration however raises concerns with respect to postoperative respiratory complications, particularly for patients undergoing large pulmonary resections. We undertook an institutional review to determine the outcome of large pulmonary resections after bleomycin-combination chemotherapy.

METHODS: Between 1981 and 2001, 530 patients presented to our institution for resection of residual intrathoracic disease for either metastatic testicular or primary mediastinal nonseminomatous germ cell tumors. We subsequently reviewed 32 of these patients who required pneumonectomy (n = 19; right = 9, left = 10) or bilobectomy (n = 13) after bleomycin-combination chemotherapy.

RESULTS: There were four operative deaths (13%). All postoperative deaths occurred in patients undergoing right-sided resections (pneumonectomy, n = 2; bilobectomy, n = 2) as a consequence of pulmonary complications. Operative survivors had a pulmonary morbidity of 18%. Fourteen of 20 long-term survivors were found to have a satisfactory performance status at follow-up.

CONCLUSIONS: Otherwise young and healthy male nonseminomatous germ cell tumors patients requiring large pulmonary resections after bleomycin-combination chemotherapy appear to be at higher than anticipated risk for pulmonary-related morbidity and mortality. However long-term survivors report an acceptable functional status.


   Introduction
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 Introduction
Material and Methods
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Nonseminomatous germ cell cancers (NSGCT) serve as premiere models for multimodality cancer therapy with cisplatin-based combination chemotherapy followed by surgical resection of residual disease. This multimodality therapy results in long-term cure rates of 80% to 90% for NSGCT of testicular origin and 50% to 60% for NSGCT primarily originating in the mediastinum [1, 2]. Bleomycin in combination with cisplatin and etoposide is believed to represent the optimal chemotherapeutic regimen for NSGCT and in particular for treatment of high-risk NSGCT cases [3, 4]. However, pulmonary toxicity, including interstitial fibrosis, is a known potential consequence of bleomycin therapy [4–6]. The potential for pulmonary toxicity raises concerns regarding postoperative pulmonary morbidity. We have previously reported low operative risks for NSGCT patients, including patients who require lobar resection [1, 2, 7]. We have, however, observed that the majority of patients experiencing operative morbidity and mortality required large pulmonary resections (pneumonectomy [PN] or bilobectomy [BL]) to remove residual disease. The purpose of this study was to review our institutional experience regarding the short-term and long-term outcomes of large pulmonary resection after bleomycin-combination chemotherapy for metastatic testicular NSGCT or primary mediastinal NSGCT.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Patient Identification
We initially reviewed our institutional records of 530 patients who underwent resection of residual intrathoracic disease after platinum-based combination chemotherapy for either metastatic testicular NSGCT (n = 422) or primary mediastinal NSGCT (n = 108) between 1981 and 2001. We identified a subset of 32 patients who required large pulmonary resections (metastatic testicular NSGCT, n = 22; primary mediastinal NSGCT, n = 10) defined as either PN or BL after bleomycin-combination chemotherapy regimens, and these patients are the basis of this report. Formal Institutional Review Board approval was obtained before hospital record review and patient contact. Our standard thoracic surgical care for NSGCT patients has been described elsewhere [1, 2]. However, to summarize, all patients received standard thoracic surgical care with aggressive perioperative pain management including epidural catheter analgesia and judicious intravenous fluid administration. Additionally, inspired oxygen concentrations were maintained at minimum levels to achieve arterial oxygen saturations of 90% or greater [3, 6, 8]. Patients were allowed at least 4 to 6 weeks of recovery after chemotherapy before surgery. Since 1992, all PN patients at our institution, including NSGCT cases, have undergone reinforcement of the bronchial stump with a rotated flap of adjacent pericardium.

Variables and Analysis
Using a structured data collection form, multiple variables were collected, including patient demographics; origin of NSGCT; chemotherapy variables including timing with respect to surgical therapy and total dose of bleomycin; surgical variables including the specific surgical approach (sternotomy, thoracotomy, or clamshell bilateral thoracotomies), type of large pulmonary resection (right or left PN, right upper and middle or middle and lower BL), and resection of other adjacent intrathoracic structures such as pericardium, phrenic nerve, great veins, and diaphragm; and pathologic category of the residual mass (necrosis, teratoma, persistent NSGCT, and non–germ cell cancer). All complications occurring during the hospitalization were recorded and categorized as pulmonary and nonpulmonary. Operative mortality was defined as death occurring within 30 days of surgery or during the hospitalization if greater than 30 days. Functional status was assessed by a nine-question survey, including functional ability according to the Eastern Cooperative Oncology Group (ECOG) scale and requirement for supplemental oxygen. Information on operative survivors was categorized as alive without evidence of disease, alive with evidence of disease, tumor-related death, non–tumor-related death, and lost to follow-up. Basic descriptive statistics for parametric and nonparametric data were used to characterize the sample when deemed appropriate. Kaplan-Meier analysis was used to calculate overall and pathologic-specific survival for operative survivors.


   Results
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 Abstract
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 Material and Methods
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Comment
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The sample was composed of all males, and the majority were young white men with a mean age at diagnosis of 27 ± 8 years. The median total dose of bleomycin was 360 IU (n = 31, range 120 to 360 IU). Bleomycin dosage was not available for 1 patient. Eighteen (60%) of the 31 patients with available chemotherapy data received a standard total dosage of 360 IU. Only 1 patient received a brief course of steroids for clinical evidence of bleomycin toxicity during chemotherapy. Six patients (19%) additionally received second-line platinum-based chemotherapy without bleomycin before surgery. Large pulmonary resections were performed after a median interval of 3.1 months (range, 0.7 to 91 months) after bleomycin-combination chemotherapy. Twenty of 32 patients (63%) underwent one thoracic surgical procedure for resection of residual disease, 9 (28%) had two procedures, and the remaining 3 patients had three or more total thoracic surgical procedures. Five of these additional thoracic surgical procedures after large resection included pulmonary wedge resection. The surgical approaches used for large pulmonary resection included thoracotomy in 25 (78%), clamshell in 5 (16%), and sternotomy in 2 (6%). Nineteen patients (59%) underwent a PN (right PN, n = 9; left PN, n = 10), and 13 (41%) underwent a BL. Nine of the BLs were middle and lower lobectomies with the remaining four involving the upper and middle lobes. Eighteen (56%) patients underwent resection of adjacent pericardium, 9 (29%) patients had resection of the ipsilateral phrenic nerve, 7 (32%) patients had partial resection of the ipsilateral diaphragm, and 4 patients (13%) had resection of a great vein. Eight (25%) of the large pulmonary resections pathologically demonstrated tumor necrosis only, 7 (22%) demonstrated benign teratoma, and 10 (31%) and 7 (22%) had elements of persistent NSGCT and degeneration into non–germ cell cancer, respectively.

The overall operative mortality was 13% (n = 4), and occurred only in patients undergoing right-sided resections (PN, n = 2; BL, n = 2, both upper and middle lobectomies); thus the operative mortality for large right-sided lung resections was 18% (4 of 22). Three of these four patients had also required phrenic nerve resection for tumor involvement. Two of 5 patients undergoing right-sided large pulmonary resection, which included en bloc ipsilateral phrenic resection, survived. All four operative deaths were attributable to acute respiratory distress syndrome (ARDS). One patient demonstrated progressive respiratory failure secondary to uncomplicated ARDS with the other three cases of ARDS complicated by secondary pneumonia (n = 1) and microscopic evidence of diffuse pulmonary arteriolar thrombi (n = 2) on postmortem examination. Patient and surgical variables in operative mortality cases are shown in Table 1. The 4 patients who died postoperatively spent an average of 14 ± 4.7 days (range, 10 to 21 days) on mechanical ventilation and were hospitalized for a mean of 17.5 ± 5.4 days (range, 10 to 22 days).


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  		Table 1. Description of Operative Deaths (n = 4)

 
Six of 28 operative survivors (21%) had one or more nonfatal complications, which are summarized in Table 2. Pulmonary complications were most common and occurred in 5 (18%) patients, including one nonfatal case of each of ARDS (n = 1) and pneumonia (n = 1). Both patients required prolonged mechanical ventilation (8 and 4 days, respectively). One additional surviving patient required reintubation for bronchoscopy and control of retained secretions. A nonfatal, nonpulmonary complication or complications occurred in 5 (18%) patients, including atrial fibrillation (n = 1), transient renal dysfunction (n = 3), and nonpulmonary sepsis (n = 3). There were no complications secondary to poor airway healing, including bronchopleural fistula. The overall average length of hospital stay in the 22 operative survivors who did not experience complications was 8.0 ±2.4 days as compared with an average of 17.4 ±7.9 days for patients experiencing one or more complications. Four of the 5 surviving patients who demonstrated pathologically persistent NSGCT in the surgical specimen and a clinical response to preoperative chemotherapy received two additional courses of cisplatin and etoposide adjuvant chemotherapy after recovery [2, 9].


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  		Table 2. Nonfatal Operative Morbiditya

 
The mean duration of follow-up was 27 months (range, 1 to 148 months) for the 28 patients who survived the surgical procedure. At the time of last follow-up, 14 (50%) were alive without disease, 5 (18%) were alive with disease, and 8 (29%) had died of disease. Only 1 patient was lost to long-term follow-up. The Kaplan-Meier survival curves for operative survivors (n = 28) and by pathologic category are shown in Figure 1. Long-term survival was dependent on pathologic category of the surgical specimen and not unexpectedly was better in patients with postchemotherapy pathologically demonstrated benign residual disease (p = 0.0026). Of the 13 patients with pathologically demonstrated benign disease, all were alive at the time of follow-up (range, 1 to 148 months).



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  		Fig 1. Long-term overall survival for patients who underwent large pulmonary resection. Curves depict long-term survival of the overall series (n = 28) and by postchemotherapy disease, benign (n = 13) versus malignant (n = 15). Numbers represent patients at risk at the 20-, 40-, and 60-month intervals for each group.

 
Fourteen of the 20 long-term survivors were available for evaluation of their functional status, and all reported an Eastern Cooperative Oncology Group functional status of either 0 (fully active and able to perform all activities without restriction, n = 5) or 1 (restricted in physically strenuous activity but ambulatory and able to carry out work of a light or sedentary nature, n = 9). One patient required supplemental oxygenation at the time of evaluation 15.8 months after surgery. This patient rated himself as an Eastern Cooperative Oncology Group status 1 at this time. No other long-term pulmonary-related morbidity or mortality has been reported.


   Comment
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Bleomycin, an antibiotic produced by the fungus Streptomyces verticillus, has been found to be useful in the treatment of a variety of neoplasms, including lymphomas and oropharyngeal malignancies, as well as germ cell tumors. The combination of cisplatin, etoposide, and bleomycin chemotherapy with subsequent surgery for residual disease has been demonstrated to be highly curative for germ cell cancers that were previously fatal shortly after diagnosis. Bleomycin causes cell death by facilitating the production of oxygen radicals, resulting in DNA chain disruption [10–12]. A hydrolase enzyme inactivates bleomycin, which is present in all tissues except the lungs and skin [13]. Pulmonary toxicity, therefore, is the predominant adverse consequence from a clinical standpoint. In animal models, bleomycin-induced pulmonary toxicity begins with endothelial cell damage, which is followed by an acute inflammatory response, including invasion of white blood cells into the interstitium [14]. Lymphocytes bound to endothelial cells activate fibroblasts to deposit collagen, which completes the process [8, 15–17].

The reported incidence of bleomycin-induced pulmonary toxicity ranges from 3% to 40% and appears to be dose related. The likelihood of clinically evident bleomycin-induced pulmonary toxicity appears to be lower if the total bleomycin dose is less than 300 to 400 IU [4–6, 8]. Bleomycin-induced pulmonary toxicity is considered to be partially reversible with steroid therapy; however, the degree of reversibility is difficult to assess, and progression has been described even after completion of chemotherapy [8, 18–21]. Although only 1 patient in this series undergoing large pulmonary resection had clinical evidence of pulmonary toxicity during bleomycin combination chemotherapy, some degree of residual nonclinically evident toxicity is of concern, as this may predispose a patient to postoperative ARDS. Donat and Levy [5] reported a 25% incidence of major postoperative respiratory problems after mostly retroperitoneal lymph node dissection for residual NSGCT disease after bleomycin combination chemotherapy in 77 patients. Such an incidence of major respiratory problems is clearly higher than would otherwise be expected in a young population. If bleomycin combination chemotherapy predisposes to postoperative ARDS after abdominal surgery, then legitimate concerns would clearly be raised in patients with similar age and sex demographics undergoing large pulmonary resections, in particular because ARDS and the so-called post-PN syndrome are already well-known and dreaded complications.

The vast majority of patients presenting with primary mediastinal NSGCT and approximately 10% to 20% of patients presenting with metastatic testicular NSGCT ultimately require a thoracic surgical procedure to remove residual disease after chemotherapy [2]. We have previously reported operative mortalities of 4% and 1%, respectively, in primary mediastinal NSGCT and metastatic testicular NSGCT patients undergoing resection of residual intrathoracic disease, with the majority of operative mortality after large anatomic pulmonary resection [1, 2, 7]. In this report, we studied a subpopulation of NSGCT patients with residual intrathoracic disease after bleomycin combination chemotherapy that required BL or PN. All operative deaths in our study were secondary to pulmonary complications, and occurred in patients undergoing right-sided resections, with an overall mortality of 13% and 18% mortality specific for right-sided resections. Pneumonectomy for non–small cell lung cancer without neoadjuvant chemotherapy can be performed with an overall reported mortality of 3% to 7%. Right PN, however, has been identified as having a significantly higher mortality primarily because of an increased frequency of the so-called post-PN syndrome as well as increased incidence of bronchial stump leakage as compared with left PN [22, 23]. Neoadjuvant non–small cell lung cancer therapy appears to be an additional risk factor for right PN. In a large retrospective study from Memorial Sloan Kettering, the 30-day mortality for right PN after neoadjuvant chemotherapy was 24%, with respiratory causes predominating [24]. The demographics as well as comorbid risk factors of patients with NSGCT obviously differ significantly from lung cancer patients. Lung cancer patients are generally in their sixth to seventh decade of life, and approximately half have preexisting comorbidities such as chronic obstructive pulmonary disease, which equates to relatively poor reserve after any type of pulmonary resection. Although risk data for large pulmonary resections in a cohort of otherwise young and healthy men are lacking, we would estimate the risks observed in our series to be three-fold to five-fold higher than expected.

As postoperative ARDS is the predominate cause of an adverse outcome, we use several common strategies to avoid this complication, which are not necessarily unique to NSGCT patients. These strategies include aggressive pain management with epidural catheter analgesia, minimizing perioperative fluids administration, and a conservative extubation policy with extubation usually deferred until the first postoperative day to avoid early atelectasis in the remaining lung parenchyma. We have also adapted several strategies, which are perhaps unique to NSGCT patients. Although small patient numbers prohibit meaningful statistical analysis, it appears that the combination of a large, right-sided pulmonary resection with en bloc removal of the ipsilateral phrenic nerve carries a higher risk. Loss of diaphragmatic function may impair breathing mechanics of the remaining contralateral lung. Many residual masses after chemotherapy for NSGCT contain no malignant elements or, if malignant elements are present, they may be more centrally located within the residual mass. We therefore avoid phrenic nerve resection if the residual disease is abutting but not involving the phrenic nerve with frozen-section control of the surgical margin [1, 2, 9]. Diaphragmatic plication after PN may be a consideration in an attempt to improve contralateral respiratory mechanics; however, plication after BL could potentially lead to pleural space complications [25].

Minimizing inspired oxygen concentrations during and after surgery is believed to have a beneficial effect on ameliorating the potential toxic effects of bleomycin [3, 6, 8]. In this regard we have more recently aggressively placed prophylactic temporary tracheostomy tubes at the time of surgery in high-risk NSGCT cases to not only facilitate ventilator weaning but also optimize secretion control. Finally, a finding of concern is the diffuse microthrombi in pulmonary arterioles in remaining lung parenchyma found on postmortem examination in 2 patients in this series. We can only speculate as to the causes of this finding, including low pulmonary blood flow as perhaps a preterminal event or related to preexisting endothelial cell damage from bleomycin. Based on these postmortem observations, however, we have also more recently used judicious anticoagulation in NSGCT patients with early clinical signs of impending ARDS.

In summary, we found an increased risk of pulmonary-related morbidity and mortality after large pulmonary resections in NSGCT patients after bleomycin combination chemotherapy regimens. Despite these relatively high risks, surgical therapy is warranted for any NSGCT patient with anatomically resectable residual disease after chemotherapy, as many NSGCT patients will achieve long-term disease-free survival even with pathologic evidence of residual malignant elements. Additionally, long-term survivors appear to have acceptable functional reserve. Our current research efforts are focused on identification of histochemical evidence of bleomycin-induced lung injury and correlation of these data with respect to dose and timing of surgery after bleomycin combination chemotherapy. Until further data are known, as bleomycin is arguably the least important component of the three-drug combination treatment regimen from an oncologic standpoint and pulmonary toxicity does appear to be dose related, we currently recommend limiting bleomycin to 300 total units if a large pulmonary resection is anticipated.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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