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Journal of Clinical Oncology, Vol 18, Issue 2 (January), 2000: 358
© 2000 American Society for Clinical Oncology

Results and Outcome of Retroperitoneal Lymph Node Dissection for Clinical Stage I Embryonal Carcinoma–Predominant Testis Cancer

By Christopher J. Sweeney, Benoit P. Hermans, Douglas K. Heilman, Richard S. Foster, John P. Donohue, Lawrence H. Einhorn

From the Department of Medicine, Division of Hematology/Oncology; Department of Urology; and Department of Medicine, Division of Biostatistics, Indiana University Medical Center, Indianapolis, IN.

Address reprint requests to Lawrence H. Einhorn, MD, Indiana University, Indiana Cancer Pavilion, 535 Barnhill Dr, Room 473, Indianapolis, IN 46202; email chsweene{at}iupui


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine the incidence of metastatic disease and usage of chemotherapy (adjuvant or metastatic) after primary retroperitoneal lymph node dissection (RPLND) in patients with clinical stage (CS) I embryonal carcinoma (EC)–predominant testicular cancer. EC predominance was defined as the presence of EC at a level greater than that of any other histologic diagonsis.

PATIENTS AND METHODS: All CS I patients with nonseminomatous germ cell tumors who underwent RPLND at Indiana University from 1990 to 1995 were reviewed retrospectively.

RESULTS: Two-year follow-up was available for 292 of 320 patients. EC-predominant disease was found in 125 (42.8%) of 292. Eighty-five (68.0%) of 125 patients with EC-predominant disease had pathologic stage (PS) I, and 18 (21.2%) of this group of 85 relapsed. A significantly lower PS I relapse rate of 3% was found for patients who had non–EC-predominant disease (P < .0001). PS II disease was more frequent in patients with EC predominance, as 40 (32.0%) of 125 had retroperitoneal metastases, compared with 26 (15.6%) of 167 patients with a non–EC-predominant histologic diagnosis (P = .0024). Chemotherapy was administered to 48 (38.4%) of the 125 patients with CS I EC-predominant disease after RPLND. This included 25 CS I patients with PS II disease who received adjuvant chemotherapy in addition to 23 patients who subsequently required chemotherapy for relapse after RPLND. Ten (66.6%) of 15 PS II EC-predominant patients were cured by surgery alone. Currently, all 125 EC-predominant patients are disease-free.

CONCLUSION: Patients with CS I EC-predominant disease are at a relatively high risk for metastatic disease.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
TESTICULAR CANCER has become a model for a curable neoplasm,1 with cisplatin-based combination chemotherapy capable of curing 75% to 80% of patients with disseminated disease.2 However, the optimal management of clinical stage (CS) I nonseminomatous germ cell tumors (NSGCT) remains controversial. By definition, patients with these tumors have normal physical examinations, abdominal and chest computed tomographic (CT) scans, and tumor markers. Historically, these patients were managed by retroperitoneal lymph node dissection (RPLND) with resultant retrograde or failure of ejaculation and consequent sterility.3 However, nerve-sparing RPLND (NSRPLND) has eliminated the historic problem with loss of emission/ejaculation. The three options that are now used are surveillance,4,5 NSRPLND,6 and primary chemotherapy for patients at high risk of relapse.7,8 Each option has advantages and disadvantages.

Histologic parameters have identified patients who are at higher risk of relapse on surveillance. Freedman et al4 found that a combination of three of the following four features was associated with a 58% chance of relapse at 2 years on surveillance: lymphatic invasion, vascular invasion, presence of embryonal carcinoma (EC), and absence of yolk sac. Sogani et al5 noted that the risk of relapse was significantly greater for patients with EC-predominant disease than for those who did not have a predominance of EC. In the study by Sogani et al, EC-predominant disease was defined as the presence of no more than a focus of another subtype of germ cell tumor. It is often argued that high-risk patients, such as those with EC-predominant disease, are not good candidates for surveillance and should be offered NSRPLND or primary chemotherapy.

We undertook this retrospective review to evaluate the clinical suspicions that patients with CS I EC-predominant disease (a) have a higher rate of extragonadal disease than those who do not have EC-predominant disease and (b) receive chemotherapy after RPLND more often, either as adjuvant therapy or for management of metastatic disease.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All patients with CS I NSGCT who underwent a NSRPLND between 1990 and 1995 were retrospectively evaluated, and all have a minimal follow-up of 2 years. Patients were considered CS I if CT scans of the chest and abdomen were normal and the tumor markers were found to be either normal or falling (three patients) in accordance with expected decay half-lives after orchiectomy. Follow-up was conducted by chart review, by writing to and/or calling the patients or the referring physician, and by reviewing the tumor registry for deaths.

All specimens were reviewed and reports were generated by pathologists at Indiana University Medical Center before the RPLND. These pathology reports were retrospectively reviewed and the histologic diagnoses were classified as EC predominant, EC present but not predominant (EC nonpredominant), and EC absent. The latter two groups were grouped together as non–EC predominant. EC predominance was defined as EC present at a level greater than any other histologic type. Different pathologists completed the reports and either listed the histologies in descending order of predominance without providing a percentage or quantified each histologic diagnosis in the specimen as a percentage of the total cancer. The pathology reports of all orchiectomy specimens were also reviewed for any mention by the pathologist of vascular invasion. Vascular invasion was categorized as present, absent, or not mentioned. Vascular invasion was considered present if the orchiectomy pathology report referred to invasion of the tumor into the lumen of lymphatic or venous vessels and was recorded as absent if this was specifically stated in the report by the pathologist.

The incidence of pathologic stage (PS) I and II disease and the ultimate use of chemotherapy (adjuvant or metastatic therapy) were determined for each classification. The rate of relapse of PS I disease and the total frequency of metastasis were determined for each group. The presence of statistical differences was evaluated by Fisher’s exact test. The number of patients who had metastases, did not receive chemotherapy, and did not relapse was also determined.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Three hundred and twenty patients with CS I NSGCT underwent RPLND at Indiana University from 1990 to 1995. A minimal 2-year follow-up was available for 292 patients (90.4%). Twenty-four patients were lost to follow-up and four had died of unrelated causes (lymphocytic myocarditis, motor vehicle accident [two patients], and work site accident). Twenty-three of the 24 patients lost to follow-up had surgery alone and had no evidence of disease when they were lost to follow-up. The remaining patient was also without evidence of disease after he had received bleomycin, etoposide, and cisplatin (BEP), having relapsed on observation for PS II disease. One hundred twenty-five (42.8%) of 292 patients had EC predominance, and 167 patients (57.8%) had non–EC predominance. The median follow-up was 46 months (range, 24 to 89 months). Only one patient has died of progressive testicular cancer. This patient had non–EC-predominant disease and died with progressive cerebral metastases 36 months after the orchiectomy.

When histologic diagnoses were recorded as percentages or foci, the percentage of EC could be evaluated for 50 (40%) of 125 EC-predominant cases and 102 (61%) of 167 non–EC-predominant cases. In the other 75 of the 125 EC-predominant cases, EC predominance was indicated by the pathologist listing EC as the most predominant histologic diagnosis without providing a percentage. Specifically, EC-predominant cases, including those with pure EC, had a mean percentage of EC of 88%, with a range of 40% to 100%. When the 22 cases of pure EC were excluded, the mean percentage of EC for the remaining 28 cases was 78%. For the 102 patients with non–EC-predominance, the mean percentage of EC was 6.45%, and when all 55 cases that had no EC were excluded, the mean percentage of EC was 14%, with a range of 1% to 50%. A specimen with 50% of one other histologic diagnosis and 50% of EC was classified as non–EC-predominant.

Rate of Relapse for PS I Disease
PS I disease was found in 226 (77.4%) of the 292 patients, 23 (10.2%) of whom relapsed and received three cycles of BEP (Table 1). Eighty-five (68.0%) of the 125 patients with EC predominance had PS I. Eighteen (21.2%) of 85 patients with EC-predominant PS I disease relapsed.


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  		Table 1. Relapse After PS I Disease
 
In contrast, 141 (84.4%) of 167 patients with non–EC predominant disease had PS I. When those with no EC were analyzed separately, 49 (89.1%) of 55 had EC-absent PS I disease, and when EC was present but not predominant, 92 (82.1%) of 112 patients had PS I disease. The rate of PS I relapse was 3% among the 167 patients in the non–EC-predominant cohort. The rate of PS I relapse was statistically greater for patients with EC-predominant disease than for those with non–EC-predominant disease (P < .0001).

Incidence of PS II Disease
The incidence of PS II disease for the entire CS I cohort was 22.4% (66 of 292 patients; Table 2). Forty (32.0%) of the 125 EC-predominant patients had retroperitoneal metastases. In comparison, 26 (15.6%) of 167 patients with CS I non–EC-predominant disease had PS II disease. PS II disease was found to occur statistically more often with EC predominance than with non–EC-predominance (P = .0024). When the subgroup with no EC in the orchiectomy specimen was analyzed separately, six (10.9%) of 55 patients had PS II disease at RPLND.


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  		Table 2. PS II Disease in CS I NSGCT (n = 292)
 
Metastatic Potential as a Function of Amount of EC
When the rate of metastatic potential is defined as either PS II or relapsed PS I disease, it is even more apparent that patients with EC-predominant disease have a greater propensity for extratesticular disease (Fig 1). Metastases were found more frequently in the EC-predominant cohort, as 46.4% of the 125 patients met this criterion, compared with 21.4% of the 112 patients with EC-present-but-not-predominant disease (EC nonpredominant) and 12.7% of those without EC (P < .00001). Fifteen (68.2%) of 22 patients with 100% EC had metastatic disease. When the metastatic rate was calculated for the EC-predominant cohort without the 22 pure EC patients, it was 41.7% (43 of 103 patients).



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  		Fig 1. Percentage of cases with metastatic disease by amount of EC. Metastatic disease (pathologic stage II or relapsed pathologic stage I) occurs statistically more often with EC predominance than with non–EC predominance and EC absence (P < .0001).

 
Chemotherapy Usage
Eighteen of 85 patients with PS I EC-predominant disease relapsed and received three cycles of BEP, and 25 of 40 PS II patients elected to receive two cycles of adjuvant BEP. It is unknown, of course, how many of these 25 patients would have been cured with surgery alone. Of the 15 patients with PS II disease who did not receive adjuvant chemotherapy, five (33.3%) relapsed and received three cycles of BEP. In all, 48 (38.4%) of 125 patients received chemotherapy (either as therapy for metastatic disease or as adjuvant therapy). Chemotherapy was instituted as adjuvant therapy for PS II disease based on the patients’ preference after being counseled on the risks and benefits. In comparison, only 18 (10.7%) of the 167 patients with non–EC-predominant disease received chemotherapy.

Effectiveness of RPLND
It should be noted that 10 (66.6%) of 15 patients with EC-predominant PS II disease were cured with surgery alone. The effectiveness of RPLND was also evidenced by the fact that only one out of 292 patients relapsed in the retroperitoneum. This patient was EC predominant with PS I disease. All the other relapses were outside the retroperitoneum, including one patient (EC nonpredominant, PS II) who relapsed in the ipsilateral obturator internal iliac lymph node, presumably because of aberrant lymphatic drainage along the vas deferens.

Vascular Invasion
Vascular invasion was documented as present in 91 patients and as absent in 87 (Table 3). The remaining 114 patients had no mention of whether vascular invasion was present or absent. Of the 91 patients with vascular invasion, 58 had EC-predominant disease and 33 had non–EC-predominant disease. EC predominance was significantly more likely to be associated with vascular invasion than was non–EC predominance (P < .001). Vascular invasion was also found to be associated with metastatic disease independent of EC status. Specifically, of the 56 patients with vascular invasion and PS I disease, 11 patients (20%) relapsed, compared with five (6.7%) out of 74 PS I patients who had no vascular invasion (P < .001). The relapse rate of those with no mention of vascular invasion status was 7.3% (seven of 96). Vascular invasion was also associated with PS II disease, as 35 (38.5%) of 91 patients with vascular invasion had involved lymph nodes, compared with 13 (14.9%) of 74 patients with no vascular invasion (P < .0001). The rate of PS II disease when vascular invasion was not mentioned was 15.8% (18 of 114 patients).


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  		Table 3. EC-Predominant Testis Cancer and Vascular Invasion (n = 178)
 
The presence of EC predominance and vascular invasion together proved to be additive with regard to the risk of metastatic disease (Table 3). Specifically, 36 (62.1%) of 58 patients with EC predominance and vascular invasion had metastatic disease, either as PS II disease (27 patients) or as relapsed PS I disease (nine patients). In contrast, the group with EC predominance and no vascular invasion had a metastatic rate of 28.1% (nine of 32 patients), and the non–EC-predominant group with no vascular invasion had a relapse rate of 16% (nine of 55 patients). It was also noted that when EC was absent and there was no vascular invasion, the metastatic rate was 5.9% (one of 17 patients). The rate of metastatic disease for patients with vascular invasion with non–EC-predominant disease was 30.3% (10 of 33 patients). This is similar to the metastatic rate for the group that had EC predominance and no vascular invasion (28%, or nine of 32 patients).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This retrospective review confirms the previous findings that EC and vascular/lymphatic invasion are predictive for an increased risk of metastatic disease. In addition, the EC-predominant subgroup is common and relevant, given the significantly increased risk for metastatic disease. The limitations of this study are that it is retrospective and the pathologists were not instructed to review the specimens a priori for the presence of EC predominance or vascular invasion, and the presence or absence of vascular invasion was not always stated in the pathology report.

It is well recognized that RPLND for all patients with CS I EC-predominant disease results in more accurate staging. This study, however, was undertaken to address our impression that chemotherapy was used more often after RPLND in patients with EC-predominant disease, either for relapsed PS I or II disease or as adjuvant therapy for PS II. It was found that 23 (18.4%) of 125 EC-predominant patients received chemotherapy for metastatic disease. In addition, 25 patients received elective adjuvant chemotherapy on confirmation of PS II disease. Primary RPLND, as part of a highly successful approach (100% survival), was successful as "monotherapy" for the 10 (66.6%) of 15 patients with PS II disease treated with surgery alone (no adjuvant chemotherapy).

There are three approaches to managing patients with CS I NSGCT, and each has advantages and disadvantages, with reported cure rates of more than 95%. Primary RPLND has been modified to the extent that in experienced hands there is almost universal preservation of ejaculation6 and the morbidity is limited to minor postoperative complications.9 It provides immediate definition of stage and eliminates the need for abdominal CT scanning in follow-up, as the rate of relapse in the abdomen is less than 2%.10 There is a higher cure rate for PS II testis cancer with surgery alone than there is for any other metastatic cancer. However, a primary RPLND is associated with a 70% incidence of negative nodes and requires expertise in the nerve-sparing technique to preserve ejaculation. In our current series, after the 25 patients who received adjuvant chemotherapy were excluded, 23 (23%) of 100 EC-predominant patients required chemotherapy after a primary RPLND.

Another management option is surveillance. The major benefit is the elimination of unnecessary treatment for the 70% of patients who do not have extratesticular disease. It requires strict compliance and the frequent use of abdominal CT scans. Investigators have shown that not all patients can comply with the required stringent follow-up. This is an important factor when discussing the options for therapy with patients with CS I disease.11,12 If a relapse does occur, patients are treated with three cycles of chemotherapy for metastatic disease and possible postchemotherapy RPLND, whereas some of those with PS II disease could have been cured by surgery alone. The most notable concern is that chemotherapy renders a patient azoospermic during therapy and recovery may be incomplete.13 Data demonstrate that most patients do recover spermatogenic capability about 2 years after therapy14 and that recovery depends on time elapsing, age, baseline semen analysis, and number of cycles and dose of chemotherapy.15 Another potential concern is the incidence of leukemia with chemotherapy. With cumulative doses of etoposide less than 2,000 mg/m2, two (0.37%) of 538 patients developed leukemia.16 By contrast, four (4.8%) of 82 with doses greater than 2,000 mg/m2 developed subsequent leukemia.17

Primary chemotherapy has the distinct advantage of having a low relapse rate with two cycles of BEP with manageable toxicities.7,8 Proponents of this approach have used this option for patients with high-risk disease. Initially, the most common criterion was the presence of one or more of the following: vascular or lymphatic invasion, EC, and no yolk sac.4 This criterion is associated with a 55% rate of relapse on surveillance and accounts for about 20% of all patients with CS I NSGCT.4,18 More recent studies have defined high-risk patients as those with vascular invasion, because of a risk of relapse on surveillance of about 40%, and this criterion accounts for about 50% of patients with CS I disease.4,18,19 Longer-term follow-up will be necessary to assess late relapses, local recurrence, incidence of second tumors, and overall survival more accurately.

In conclusion, patients with CS I EC-predominant disease are at a higher risk for metastatic disease than those with non–EC-predominant disease. Of this 125-patient cohort with EC-predominant disease, 48 patients (38.4%) received chemotherapy after RPLND, including 23 patients (18.4%) who received treatment for relapse after RPLND and 25 patients (20%) who elected adjuvant chemotherapy after discovery of PS II disease. Furthermore, 21.2% with PS I disease relapsed. Presentation with EC-predominant disease is therefore common in CS I NSGCT and relevant because of the high risk of metastatic disease.


   ACKNOWLEDGMENTS
 
Supported in part by National Cancer Institute grant no. 2 R 35 CA 39844-14 and the Walther Cancer Institute, Indianapolis, IN.


   NOTES
 
Presented in part at the Thirty-Fourth Annual Meeting of the American Society of Clinical Oncology, Los Angeles, CA, May 16-19, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Einhorn LH: Testicular cancer as a model for a curable neoplasm. Cancer Res 41:3275-3280, 1981[Medline]

2. Bosl GJ, Motzer RJ: Testicular germ cell cancers. N Engl J Med 337:242-253, 1997[Free Full Text]

3. Narayan P, Lange PH, Fraley EE: Ejaculation and fertility after extended retroperitoneal lymph node dissection for testicular cancer. J Urol 127:685-688, 1982[Medline]

4. Freedman LS, Parkinson MC, Jones WG, et al: Histopathology in the prediction of relapse of patients with stage I testicular teratoma by orchiectomy alone. Lancet 2:294-297, 1987[Medline]

5. Sogani PC, Perrotti M, Herr HW, et al: Clinical stage I testis cancer: Long term outcome of patients on surveillance. J Urol 159:855-858, 1998[Medline]

6. Donohue JP, Thornhill JA, Foster RS, et al: Retroperitoneal lymphadenectomy for clinical stage I testis cancer (1965-1989): Modifications of technique and impact on ejaculation. J Urol 149:237-243, 1993[Medline]

7. Cullen MH, Stenning SP, Parkinson MC, et al: Short course of adjuvant chemotherapy in high risk stage I non-seminomatous germ cell tumors of the testis (NSGCTT): An MRC study report. Proc Am Soc Clin Oncol 14:244, 1995 (abstr)

8. Pont J, Albrecht W, Postner G, et al: Adjuvant chemotherapy for high-risk clinical stage I non-seminomatous testicular germ cell cancer: Long-term results of a prospective trial. J Clin Oncol 14:441-448, 1996[Abstract/Free Full Text]

9. Baniel J, Foster RS, Rowland R, et al: Complications of primary retroperitoneal lymph node dissection. J Urol 152:424-427, 1994[Medline]

10. Donohue JP, Thornhill JA, Foster RS, et al: Primary retroperitoneal lymph node dissection in clinical stage A non-seminomatous germ cell testis cancer: Review of the Indiana University experience 1965-1989. Br J Urol 71:326-335, 1993[Medline]

11. Hao D, Seidel J, Brant R, et al: Compliance of clinical stage I nonseminomatous germ cell tumor patients with surveillance. J Urol 160:768-71, 1998[Medline]

12. Young BJ, Bultz BD, Russell JA, et al: Compliance with follow-up of patients treated for non-seminomatous testicular cancer. Br J Cancer 64:606-608, 1991[Medline]

13. Drasga RE, Einhorn LH, Willams SD, et al: Fertility after chemotherapy for testicular cancer. J Clin Oncol 1:179-183, 1983[Abstract]

14. Lange PH, Narayan P, Vogelzang NJ, et al: Return of fertility after treatment for nonseminomatous testicular cancer: Changing concepts. J Urol 129:1131-1135, 1983[Medline]

15. Petersen PM, Hansen SW, Giwercmann A, et al: Dose dependent impairment of testicular function in patients treated with cisplatin-based chemotherapy for germ cell tumors. Ann Oncol 5:355-358, 1994[Abstract/Free Full Text]

16. Nichols CR, Breeden ES, Loehrer PJ, et al: Secondary leukemia associated with a conventional dose of etoposide: Review of serial germ cell tumor protocols. Inst 85:36-40, 1993[Abstract/Free Full Text]

17. Pedersen-Bjergaard J, Daugaard G, Werner Hansen S, et al: Increased risk of myelodysplasia and leukemia after etoposide, cisplatin and bleomycin for germ cell tumors. Lancet 331:359-363, 1991

18. Read G, Stenning SG, Cullen MH, et al: Medical Research Council Prospective Study of Surveillance for stage I testicular teratoma. J Clin Oncol 10:1762-1768, 1992[Abstract/Free Full Text]

19. Dearnaley DP, Fossa SD, Kaye SJ, et al: Adjuvant bleomycin, vincristine and cisplatin for high risk clinical stage I (HRCS1) non-seminomatous germ cell tumors (NSGCT): A Medical Research Council (MRC) Pilot Study. Proc Am Soc Clin Oncol 17:309, 1998 (abstr)

Submitted January 4, 1999; accepted July 27, 1999.




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