ORIGINAL ARTICLES: GENERAL THORACIC

Pulmonary Metastasectomy for Testicular GermCell Tumors: A 28-Year ExperienceDavid Liu, MD, Amir Abolhoda, MD, Michael E. Burt, MD, PhD, Nael Martini, MD,Manjit S. Bains, MD, Robert J. Downey, MD, Valerie W. Rusch, MD,George J. Bosl, MD, and Robert J. Ginsberg, MDThoracic Service, Department of Surgery, Genitourinary Oncology Service, Division of Solid Tumor Oncology, and Department ofMedicine, Memorial Sloan-Kettering Cancer Center, New York, New York

Background. The role of surgery in patients with pul-monary metastatic germ cell tumors has been evolvingsince the 1970s. To evaluate the results of pulmonaryresection, we reviewed our 28-year experience.

Methods. Between July 1967 and May 1995, 157 patientswith testicular germ cell tumors underwent pulmonaryresections for suspected metastases. Their clinical andpathological data were reviewed. Kaplan-Meier and Coxregression models were used to analyze prognostic fac-tors for survival after resection of metastatic disease.

Results. All patients were male with median age of 27years (range 15–65). Complete resection was accom-plished in 155 (99%) patients. Viable carcinoma waspresent in 44% (70) of the patients. Forty-one (26%)

patients had metastases to other sites after pulmonarymetastasectomy. The overall actuarial survival 5 yearsafter pulmonary resection was 68% for the entire groupand 82% for patients diagnosed after 1985. On multivar-iate analysis, the adverse prognostic factors were metas-tases to nonpulmonary visceral sites (p 5 0.0069) and thepresence of viable carcinoma in the resected specimen(p < 0.0001).

Conclusions. With current chemotherapy regimens, al-most 85% of the patients with testicular germ cell tumorsundergoing complete resection of their pulmonary me-tastases can be expected to achieve long-term survival.

(Ann Thorac Surg 1998;66:1709–14)© 1998 by The Society of Thoracic Surgeons

Germ cell tumors (GCT) are uncommon neoplasmsaccounting for 1% of all cancers, but are the most

common malignancy in young adult males between theages of 15 and 35 years [1]. Ninety percent of thesetumors arise from the testes. The current annual inci-dence of GCT is approximately 5 cases per 100,000. Whilethe incidence of GCT has been steadily increasing, themortality rate from GCT has declined [2] which has beenattributed to the advent of an effective multimodalityapproach consisting primarily of cisplatin-based chemo-therapy and surgery. The prognosis of patients withGCT, including those patients with distant metastaticspread (most commonly lung [3]), is excellent. Surgicalresection of residual disease after chemotherapy plays animportant adjunctive role in the management of germcell tumors. We report our experience with pulmonarymetastasectomy and its role in the multimodality therapyof GCT.

Material and Methods

Between July 1967 and May 1995, 2,138 patients withnewly diagnosed GCT were seen at the Memorial Sloan-

Kettering Cancer Center. One thousand eight hundredpatients had testicular primaries. Approximately 30% ofthese patients developed intrathoracic lesions. Duringthis time period, 168 patients with testicular GCT hadradiographic evidence of intrathoracic abnormalities af-ter chemotherapy and underwent thoracic explorationwith either diagnostic or therapeutic intentions. We ex-cluded patients who had mediastinal disease and identi-fied 157 patients with intrathoracic lesions limited to thelungs who are the subjects of this study. Operativeindications were as follows: patients who had (1) com-plete serologic response with residual pulmonary lesions,(2) evidence of persistent intrathoracic disease with ele-vated tumor markers despite a full course of chemother-apy, or (3) lesions which did not respond or progressedwhile on chemotherapy. Complete clinical and patho-logic data were reviewed. Serum tumor markers, a-feto-protein (AFP) and human chorionic gonadotropin(HCG), were recorded if obtained within 3 weeks beforetheir surgery. Clinical outcome was measured from thetime of the first thoracic operation to the date of the firstrecurrence and to the date of either the last follow-up ordeath. Categories at the time of the last follow-up wereno evidence of disease, alive with disease, died of othercauses, and died of disease.

All statistical analyses were performed using SPSS 6.1for Windows (SPSS Inc, Chicago, IL). The Kaplan-Meierand Cox regression methods were used to analyze prog-nostic factors for survival after resection of metastatic

Presented at the Thirty-fourth Annual Meeting of The Society of ThoracicSurgeons, New Orleans, LA, Jan 26–28, 1998.

Address reprint requests to Dr Ginsberg, Division of Thoracic Surgery,Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, C-881, NewYork, NY 10021 (e-mail: GinsbergR@mskcc.org).

© 1998 by The Society of Thoracic Surgeons 0003-4975/98/$19.00Published by Elsevier Science Inc PII S0003-4975(98)00940-0

disease. A p value of less than 0.05 was regarded asstatistically significant.

DiagnosisAll patients were male. Their ages ranged from 15 to 65years, with a median of 27 years. Ninety-seven percent ofthe testicular primary tumors (n 5 153) were nonsemi-nomas. Forty-nine patients had pure embryonal cellcarcinoma which accounted for almost one third of allhistologies, 46 had a mixed pattern, 34 had teratocarci-nomas, and 24 had mature teratomas (Table 1).

Nearly half the patients (n 5 71) presented with syn-chronous metastases. For those patients who developedmetastases subsequently, the median interval from thetime of initial diagnosis was 8 months with a range from1 to 175 months. Forty-three patients had solitary metas-tases. The remainder had 2 or more metastases with amedian number of 4 and a range of 2 to 27. Of thepatients with multiple lesions, 61 had lesions confined toone lung, and 53 had lesions involving both lungs.

TreatmentAll 157 patients in this review had undergone an inguinalorchiectomy for their primary testicular lesion and 153patients were then treated with systemic chemotherapy.Of these, 143 patients received cisplatin-based chemo-therapy. Four patients received only external radiation tothe retroperitoneum and inguinal regions after orchiec-tomy. In addition to chemotherapy, 85 patients under-went retroperitoneal lymph node dissections, 25 of whichwere performed either concurrently with their pulmo-nary resections or during the same hospital stay. Nine-teen patients had disease involving other organs andlocal control was obtained before undergoing pulmonaryresection. The remaining 138 patients had hematogenousspread limited to the lung.

One hundred two patients had serum tumor markersassessed within 3 weeks before their surgery. The serol-ogy was normal in 94 patients. Eight patients had ele-vated serum tumor markers defined by AFP . 15 ng/mL,HCG . 2 ng/mL or 2.2 mIU/mL. Viable tumor in theresected specimens was found in 5 (63%) of 8 patientswith positive serologies compared with only 11 (12%) of94 patients with normal serum tumor markers.

The operative approach at the initial thoracotomy wasunilateral in 104 patients and bilateral in the remainder

either by a median sternotomy (n 5 20), clamshell (n 522), or staged bilateral thoracotomies (n 5 11). Conser-vation of pulmonary parenchyma when possible was therule reflected by the fact that most resections wereconfined to wedge excisions (n 5 141). Fourteen patientshad a lobectomy and 2 patients required a pneumonec-tomy. All patients underwent resection with curativeintent except for 2 patients who were found to haveunsuspected mediastinal disease in addition to theirpulmonary lesions. There was one postoperative deathsecondary to pneumonia. Ten patients had complicationsafter surgery, the most common being prolonged airleaks (n 5 5). Other complications included one aorticinjury, one partial esophageal tear, one stroke, and twoseptic complications. The overall mortality rate was 0.6%and morbidity rate 6%.

Results

HistologyHistologic examination of the resected pulmonary spec-imens revealed viable tumor in 70 patients, necrosis/fibrosis in 47 patients, and mature teratoma in 40 pa-tients. Sixty-three patients (40%) had histology from theirresected pulmonary lesions that agreed with the histol-ogy from their testicular primary (Table 1). Interestingly,mature teratoma in the resected pulmonary lesions wasfound in 7 patients who had pure embryonal carcinomain their primary histology. Of the 25 patients who under-went RPLN dissection and pulmonary resection eithersimultaneously or during the same hospital stay, 6 (24%)had discordant pathologies between the pulmonary andretroperitoneal specimens.

RecurrenceSeventy-three patients remained disease free after theirfirst thoracic operation and 58 patients developed recur-rences with the majority being located in the lungs.Nonpulmonary visceral sites of recurrence includedbrain, retroperitoneum, neck, liver, and other sites (Table2). Seventy-four percent of patients (n 5 43) who hadrecurrence of disease did so within 1 year (median, 5months). Thirty-three patients (58%) who had recur-rences and both patients who had unresectable diseasedied.

Table 2. Site of Recurrences After Pulmonary Resection(n 5 58 patients)

Location No. of sites

Lung 34Brain 10Retroperitoneum 8Neck 4Intraabdominal 4Liver 4Bone 3Other (atrium, testis) 4

Table 1. Histology of the Testicular Primary and ResectedPulmonary Lesions

Histologic TypeViableTumor

Fibrosis/Necrosis

MatureTeratoma

No. ofpatients

NonseminomasPure embryonal cell 29 13 7 49Teratocarcinoma 10 10 14 34Mature teratoma 14 3 7 24Mixed type 15 19 12 46

Seminomas 2 2 0 4Total 70 47 40 157

1710 LIU ET AL Ann Thorac SurgPULMONARY METASTASECTOMY FOR TESTICULAR GCT 1998;66:1709–14

SurvivalThe overall survival at 5 years was 68% and remainedessentially unchanged thereafter (Fig 1). One hundredpatients are currently alive without evidence of disease(NED) and 6 with recurrent disease. Forty-seven patientsdied of disease and 3 patients died of other causesincluding sepsis, complications of acute myelogenousleukemia, and bladder carcinoma. The median follow-upwas 38 months.

Since 1975, all chemotherapy was cisplatin-based. The143 patients who received this chemotherapy had a5-year survival rate of 71% whereas the 14 patients whoreceived a non–cisplatin-based regimen or no chemo-therapy had a 5-year survival rate of 42% ( p 5 0.0009).

Serum tumor markers within 3 weeks of surgery wererecorded in 102 patients. Five (62%) of 8 patients withpositive serologies and 75 (80%) of 94 patients withnegative serologies were alive without disease with amedian follow-up time of 82 months and 46 months,respectively ( p 5 0.21).

Patients with residual viable tumor had a significantlyworse prognosis when compared with patients who hadfindings of necrosis/fibrosis or mature teratoma. Overall10-year survival for patients with viable carcinoma was43% compared with 86% and 84% for patients withnecrosis/fibrosis and mature teratoma, respectively ( p ,0.0001) (Fig 2).

One hundred sixteen patients had metastatic diseasethat was limited to either the lungs or lungs and retro-peritoneum. The 5-year survival rate in this group was77%. The remaining 41 patients who had involvement atsites other than lungs or the retroperitoneum had asignificantly lower 5-year survival rate of 47% ( p 50.0001) (Fig 3).

Various factors were analyzed for prognostic signifi-cance. These include age, disease-free interval after treat-ment of primary, primary histology, preoperative serumtumor markers, number of pulmonary metastases, num-ber of lesions with viable tumor, location of metastases,presentation of pulmonary metastases (synchronous ver-sus metachronous), extent of disease, type of chemother-apy, and pathology of resected pulmonary lesions (Table

3). On univariate analysis, the factors which were signif-icant for worse survival were patients more than 25 yearsof age ( p 5 0.048), patients who did not receive cispla-tin-based chemotherapy ( p 5 0.0009), patients who hadcancer in their resected pulmonary lesions ( p , 0.0001),and patients who had extrathoracic involvement as well,other than the retroperitoneum ( p 5 0.0001). On multi-variate analysis, only patients who had viable tumor intheir lungs at the time of thoracotomy ( p , 0.0001) andpatients who had nonpulmonary visceral metastases (p 50.0069) had significantly worse survival rates.

Comment

The lung is the most common site of metastases inpatients with disseminated disease from testicular GCTs.These patients undergoing pulmonary resection have thebest survival when compared with patients with metas-tases from other tumor types including epithelial tumors,sarcomas, and melanomas, resulting in 5-year survivalrates of 68% [25]. For such patients, resection of metas-tases is routinely considered after completion of cispla-tin-based chemotherapy. Surgical resection of residualpulmonary disease has an important role in determiningthe response to chemotherapy and identifying thosepatients that should receive additional chemotherapy (ie,presence of viable malignant tumor).

Fig 1. Overall survival of patients after pulmonary resection.Fig 2. Overall survival according to histology of resected specimens.

Fig 3. Overall survival according to metastatic sites involved.

1711Ann Thorac Surg LIU ET AL1998;66:1709–14 PULMONARY METASTASECTOMY FOR TESTICULAR GCT

The role of pulmonary metastasectomy in the treat-ment of testicular GCT has been evolving with theintroduction of cisplatin to chemotherapy regimens inthe mid-1970s. Further advances were made in the mid-1980s with the introduction of new technology, betterdetection methods, and treatment protocols. The im-provements in the overall survival of patients undergoingpulmonary resection for their metastatic lesions reflectsthese periods. In the pre-cisplatin era (1967–1974), the5-year survival rate for patients after pulmonary resec-tion was 41%. After cisplatin was introduced and becamea standard component in the medical treatment of pa-tients with metastatic disease, the 5-year survival rateimproved to 65%. Patients diagnosed after 1985 had a5-year survival rate of 82% ( p , 0.0001) (Fig 4). Thislatter improvement is most likely due to stage migration[4].

One of the significant prognostic factors in our analysiswas the pathology of the resected pulmonary specimens.Numerous studies have demonstrated the prognosticvalue of the histology of the resected residual lesions.Toner and colleagues examined 185 patients who under-went surgery within 6 months of completing chemother-apy [5]. In 157 patients who underwent retroperitonealresections after chemotherapy, patients who had residualmalignancy fared worse than patients who had necroticdebris or teratoma in their resected specimens. Einhornand colleagues examined the role of surgical resection indisseminated testicular cancer after chemotherapeuticcytoreduction [6]. Twenty-one patients underwent surgi-cal resection for residual pulmonary lesions and 41 pa-tients underwent lymphadenectomy for persistent retro-peritoneal disease. Thirty-five of 39 patients with benignpathology remained continuously free of disease with aminimum postoperative follow-up time of 6 months. Incontrast, only 2 of 22 patients with resected carcinomasremained continuously free of disease. Similarly, in astudy by Fosså and associates, 83 of 89 patients withbenign pathology were without evidence of disease aftera median observation of 55 months [7]. Only 7 of 12patients with malignant tumor in the operative specimensurvived without evidence of disease. In our study, 73(84%) of 87 patients with complete necrosis and/or fibro-sis or mature teratoma are alive and well, whereas only27 (39%) of 70 patients with viable malignant tumor intheir resected lesions are alive and well at last follow-upwith a median observation of 38 months (Table 4).

About 15% to 20% of all resected residual masses(pulmonary and retroperitoneal) contain viable GCT, andthe remainder contain either necrosis/fibrosis or matureteratoma in about equal percentages [5, 8]. Interestingly,the percent of residual masses containing viable tumor ishigher in pulmonary residual lesions than in retroperi-toneal masses [6, 9–11]. In these studies, carcinomaaccounted for approximately 31% to 52% of all patholo-gies compared with 42% in our study.

Several studies have attempted to predict the histologyof the residual lesions preoperatively in order to spare

Table 3. Results of Univariate and Multivariate Analysis

VariablesNo. of

PatientsUnivariate

p ValueMultivariate

p Value

Age (y)# 25 71 0.048 0.069. 25 86

Disease-free interval (mo)# 6 100 0.72. 6 57

Primary histologySeminoma 4 0.96Nonseminoma 153

Cisplatin-based chemotherapyYes 143 0.0009 0.075No 14

Preoperative tumor markersNormal 84 0.21Elevated 18

No. of pulmonary metastasesSolitary 43 0.73Multiple 114

Lesions with viable tumorSolitary 28 0.73Multiple 42

Location of metastasesUnilateral 104 0.26Bilateral 53

Presentation of metastasesSynchronous 71 0.61Metachronous 86

Extent of disseminateddiseaseLung only 116 0.0001 0.0069Lung 1 other sites (brain,

neck, liver,gastrointestinal, bone)

41

Pathology of resected lesionsCancer 70 , 0.0001 , 0.0001Mature teratoma 40Fibrosis/necrosis 47

Fig 4. Overall survival of patients according to year of primary di-agnosis.

1712 LIU ET AL Ann Thorac SurgPULMONARY METASTASECTOMY FOR TESTICULAR GCT 1998;66:1709–14

those patients with benign pathology from operation [7,12–15]. Various predictor factors have been assessedincluding size of lesion before and after chemotherapy,histology of primary tumor, tumor markers, findings oncomputed tomographic scan, and most recently positronemission tomography scan. None have demonstrated areliability in predicting preoperatively which massescontain necrosis/fibrosis, mature teratoma, or viable ma-lignant tumor. When the pathologies between the retro-peritoneal residual thoracic masses were compared,there were discordant findings ranging from 25% to 46%[11, 16–18]. In our study, 6 of 27 patients had dissimilarpathologies for a discordant rate of 22%. Therefore,pathologic findings from one site cannot be reliably usedto predict the histology of another site. It is unclearhowever, whether or not resection of all lesions is neces-sary. Watchful waiting may be another option.

Traditionally, patients with elevated serum markers,indicative of persistent disease were believed to be un-resectable and not considered for surgical resection.However, a few studies have demonstrated the potentialfor cure with salvage surgery in a select group of patients.Patients who were most likely to benefit from pulmonaryresection of chemoresistant disease had lesions whichwere limited to one site and completely resectable. In astudy by Murphy and colleagues, 3 of 4 patients withdisease limited to the lung parenchyma and 1 of 2patients with mediastinal nodal disease only, had noevidence of disease with a minimal follow-up time of 31months [19]. In another report by Wood and colleagues[20], 3 patients with lung metastases and 1 with medias-tinal disease were resected. Two were free of disease 16months later. Eight patients in our study had persistentlyelevated serum tumor markers after chemotherapy priorto undergoing pulmonary resection. Five were alive with-out evidence of disease, 3 of whom are considered to becured with follow-up times greater than 15 years. Whilethe number of patients in this group is too small to drawdefinitive conclusions, long-term disease free status ispossible with salvage surgery.

The other significant prognostic factor of outcome inour study was involvement of extrathoracic sites otherthan the retroperitoneum. It is generally recognized thatthe lung and retroperitoneum are favorable sites formetastases whereas nonpulmonary visceral metastasespredict poor prognosis. Various staging systems includ-ing one proposed by the International Germ Cell Cancer

Collaborative Group have designated patients with non-pulmonary visceral metastases as being in the poor riskcategory [21]. In their study, the presence of liver, bone,brain, or other nonpulmonary visceral metastases wereeach associated with 5-year survival rates below 50%.When grouped together, patients with any nonlung vis-ceral metastases had an overall 5-year survival rate of41% compared with 83% for patients who had diseaselimited to the lung or retroperitoneum. In our study, 125patients had metastatic disease limited to either the lungsalone or lungs and retroperitoneum. The 5-year survivalrate in this group was 77%. The remaining 43 patientswho had involvement at sites other than lungs or retro-peritoneum had a significantly lower 5-year survival rateof 40% (Fig 3).

Our current treatment of good-risk GCT patients withpulmonary metastases consists initially of combinationcisplatin-based chemotherapy [22, 23]. Of the patientswho relapse from a complete remission, fewer than 25%can be salvaged by ifosfamide and cisplatin-based regi-mens [24]. A significant number of patients with pulmo-nary metastases manifest residual radiographic abnor-malities in the lung despite normal markers afterchemotherapy. Because there is no reliable method ofpredicting the histology of the residual lesions, surgicalresection of all sites of metastatic disease is indicated inthis select group of patients.

Postoperative management depends on the pathologyof all resected masses. No further treatment is warrantedwith pathological confirmation of fibrosis/necrosis andmature teratomas. Approximately 90% of these patientswill be cured with resection alone. The identification ofviable malignant tumor in any resected lesion necessi-tates further treatment with chemotherapy [6]. Sixty to70% of patients are cured with this approach. The 30% ofpatients who fail treatment have a poor prognosis andshould be considered for experimental high-dose chemo-therapy trials or other innovative treatment strategies.Salvage surgery should only be considered for the veryrare patients with persistently elevated serum tumormarkers after a full course of chemotherapy who haveresectable metastases limited to the lung.

Conclusions

Currently, patients with testicular germ cell tumors un-dergoing complete resection of pulmonary metastasesafter cisplatin-based chemotherapy are expected toachieve long-term survival. Patients with nonpulmonarymetastases, persistently elevated tumors markers, or vi-able tumor at the time of thoracotomy have a worseprognosis. Pulmonary resection has an important role insalvage surgery for patients with chemorefractory tumorsand in identifying those patients with persisting viabletumor requiring further treatment.

References

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Table 4. Status of Patients According to Histology ofResected Specimens

Viable Tumor Necrosis/Fibrosis Mature Teratoma

AWD 2 3 1DOC 3 1 0DOD 38 5 4NED 27 38 35Total 70 47 40

AWD 5 alive with disease, DOC 5 died of other causes, DOD 5died of disease, NED 5 no evidence of disease.

1713Ann Thorac Surg LIU ET AL1998;66:1709–14 PULMONARY METASTASECTOMY FOR TESTICULAR GCT

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DISCUSSION

DR HARVEY I. PASS (Detroit, MI): I am curious as to whetheryou can decrease your operations and predict whether you havefibrosis or no viable tumor. At your institution, do you have anydata prospectively in these patients of preoperative positronemission tomography scanning and then correlative pathologyafter you have operated on these patients to see if positronemission tomography scanning could predict who was reallygoing to have a viable tumor or not? Thank you.

DR LIU: There has been a study done looking at the use ofpositron emission tomography scanning to predict the histologyof the pulmonary lesions. Other investigators have looked atvarious modalities and factors including computed tomographyscans, the histology of the primary, and the histology from theretroperitoneal node dissections. None of them have been ableto demonstrate a reliable way of predicting the histology of thepulmonary lesions.

1714 LIU ET AL Ann Thorac SurgPULMONARY METASTASECTOMY FOR TESTICULAR GCT 1998;66:1709–14