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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.11.023 on June 14, 2004

Annals of Surgical Oncology 11:658-664 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Outcomes After Combined Therapy Including Surgical Resection in Patients with Epithelial Ovarian Cancer Recurrence(s) Exclusively in Lymph Nodes

Catherine Uzan, MD, Philippe Morice, MD, Annie Rey, BS, Patricia Pautier, MD, Sophie Camatte, MD, Catherine Lhommé, MD, Christine Haie-Meder, MD, Pierre Duvillard, MD and Damienne Castaigne, MD

From the Departments of Surgery (CU, PM, SC, DC), Biostatistics (AR), Medical Oncology (PP, CL), Radiotherapy (CH-M), and Pathology (PD), Institut Gustave Roussy, Villejuif, France.

Correspondence: Address correspondence and reprint requests to: Philippe Morice, MD, Service de Chirurgie, Institut Gustave Roussy, 39 rue Camille Desmoulins, 94805 Villejuif Cedex, France; Fax: 33-1-42-11-52-13; E-mail: morice{at}igr.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The aim was to study the prognosis for and survival of patients treated with combined therapy (including surgical resection) for nodal recurrences from epithelial ovarian cancer (EOC).

Methods: This was a retrospective study of a group of 12 patients with a recurrence from EOC, a priori, exclusively located in lymph node(s). All patients underwent surgical resection of nodal metastases, followed by adjuvant therapy.

Results: The median age of patients was 51 (range, 42–71) years. The initial disease stages were as follows: stage IA, n = 5; stage IIA, n = 1; and stage IIIC, n = 6. The median interval between the end of initial treatment and the nodal relapse was 21 (range, 6–72) months. The recurrence was located in the abdominal nodes in 10 patients (pelvic and/or para-aortic area) and was extra-pelvic in one patient, and the last patient had concomitant para-aortic and supraclavicular nodal involvement. Ten patients received postoperative chemotherapy and two had radiation therapy (one patient received both treatments). Eight patients relapsed and four did not. To date, three patients have died of the disease, three are alive with persistent disease, and six are alive and disease-free (including two patients who were treated by surgical resection after relapses twice in abdominal nodes). Five-year overall survival from the time of treatment of recurrent disease is 71% (confidence interval, 41%–90%).

Conclusions: The prognosis of patients with an a priori isolated nodal recurrence from EOC was good in this group of treated with surgical resection followed by chemoradiation or radiation therapy. This finding argues in favor of proposing surgical resection in such patients.

Key Words: Lymphadenectomy • Nodal recurrence • Ovarian cancer • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The major role of primary cytoreductive surgery in epithelial ovarian cancer (EOC) is well established.1,2 A meta-analysis recently published by Bristow2 provided evidence that maximal cytoreduction was one of the most powerful determinants of cohort survival among patients with stage III or IV ovarian carcinoma. However, the place of systematic pelvic and para-aortic lymphadenectomy at the time of initial surgery is currently being debated. In patients with early-stage disease (stage I, according to the FIGO classification), the rate of positive nodes varies from 2% to 20%.3,4 In such cases, this procedure could help to identify a subgroup of patients who would benefit from adjuvant therapy if lymphadenectomy is performed. In patients with advanced-stage disease, the strongest prognostic factor is the size of the residuum at the end of debulking surgery.2

As EOC is one of the most lymphophilic pelvic tumors, pelvic and para-aortic lymphadenectomies should, in theory, be performed if tumor resection is to be complete. However, no randomized study has demonstrated the therapeutic value of surgical resection of positive nodes in such patients. A recent randomized study, yet to be published but presented during a recent meeting, seems to suggest that disease-free survival is significantly increased in patients with stage III or IV disease who undergo a complete lymphadenectomy compared to patients who simply undergo resection of bulky nodes (83% versus 63% at 3 years).5 Such results could be a strong argument in favor of proposing systematic pelvic and para-aortic lymphadenectomies for patients who are optimally debulked (residual disease <1 cm in the abdomino-pelvic cavity). Unfortunately, the overall survival rates were similar in both groups in that study.5

In the literature, the place of lymphadenectomy at the time of initial treatment of patients with EOC is still being debated, but no article has assessed the prognosis and survival of patients with a nodal recurrence treated at least by surgical resection. The aim of this study was to evaluate the prognosis and therefore to discuss the place of surgery in patients with a recurrence from EOC a priori limited to lymph nodes.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
We reviewed the data concerning EOC patients treated between June 1987 and November 2000 whose first histologically confirmed relapse was, a priori, located exclusively in lymph node(s). This recurrence developed after an interval of ≥6 months after the end of treatment of the initial tumor. Patients with at least one of the following criteria were excluded from this analysis:

All patients underwent surgical resection of the positive node(s). Postoperative treatment was administered, but the modality was dependent on the date of treatment during the study period; the characteristics of the nodal metastasis (number, presence or absence of capsular rupture, location of the node(s), associated extranodal spread); previous treatment (and treatment modality); and the patient’s medical status.

Patients’ characteristics at the time of the initial treatment (disease stage, surgical procedures, size of the residuum, adjuvant treatment modality) were studied. Concerning the characteristics of the nodal recurrence, we analyzed the duration of the clinical remission (defined as the time from the end of the first treatment to the clinical diagnosis of the nodal recurrence), the method used to diagnose the recurrence, the site, the treatment used (characteristics of the surgical procedure, postoperative therapy), and the survival of patients.

Overall survival and survival after the first relapse were calculated with use of the Kaplan-Meier method.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the study period, 12 patients had an a priori isolated nodal recurrence from EOC. Eight patients were initially treated outside our institution and were referred to us for recurrent disease, and four patients were treated in our institution. The median age of patients was 51 (range, 42–71) years.

Characteristics of the Initial Tumor
Patient characteristics are detailed in Table 1Go. The initial disease stages (according to the 1987 FIGO classification) were as follows: stage IA, n = 5; stage IIA, n = 1; and stage IIIC, n = 6 (without peritoneal disease in 2). Two patients had stage IIIC disease on the basis of histologic examination of the lymphadenectomy specimen. All patients underwent, at least, a hysterectomy with bilateral salpingo-oophorectomy, omentectomy, multiple peritoneal biopsies, and peritoneal effusion cytology. Nine patients had initial surgery without a pelvic or para-aortic lymphadenectomy (8 patients initially treated outside our institution and a 71-year-old patient treated in our institution). Among these 9 patients, 4 were considered as having stage I disease (cases 1, 5, and 12) or stage II disease (case 3) on the basis of the histologic analysis of the peritoneal specimens (but without analysis of lymph that were not resected during initial surgery). One patient initially treated outside our institution underwent a pelvic lymphadenectomy alone (without para-aortic dissection) at the time of initial surgery. The size of the residuum at the time of initial surgery was not applicable (complete macroscopic resection) in 7 patients; <2 cm in 4 patients; and >2 cm in the last one. Nine patients received adjuvant chemotherapy (platinum-based in all patients, including paclitaxel in 4 patients). The histologic subtype of the initial tumor was serous in eight patients (67%) and endometrioid in four (33%; one of them had a mixed subtype with endometrioid and clear cells).


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  		TABLE 1. Patient characteristics
 

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  		TABLE 2. Patient characteristics (continued)
 
Characteristics of the Nodal Recurrence
The median disease-free interval (between the end of the initial treatment and the nodal relapse) was 21 (range, 6–72) months. The sites of recurrent disease are presented in Table 1 Go. The nodal recurrence was located in abdominal nodes in 10 patients (pelvic area in 4, para-aortic area in 5, and both areas in 1 patient, and it was associated with peritoneal carcinosis in 1 of these 10 patients); it was extrapelvic in 1 patient (isolated inguinal node), and the last patient had concomitant para-aortic and supraclavicular nodal recurrences. The diagnosis of recurrent disease was based on the clinical examination and an elevated CA 125 level in two patients (cases 5 and 9); an elevated CA 125 level and then a suspicious lesion diagnosed on imaging studies (9 cases); and isolated elevation of CA 125 in the remaining patient. Two patients had positive positron emission tomography (PET) images.

For the surgical treatment of the nodal recurrence, a laparotomy was performed in 10 patients (9 had no visible peritoneal disease and 1 [case 2] had minimal peritoneal carcinosis that was removed at resection of the nodal recurrence). A complete macroscopic resection of suspicious nodes was performed in all cases. A single localized adenectomy was performed in five cases for recurrent disease that occurred in three patients who underwent a lymphadenectomy during the initial treatment and in two patients with extra-abdominal involvement (supraclavicular or inguinal nodes). However, in one of the latter two patients (case 9), a laparoscopic procedure was performed in order to verify the absence of peritoneal disease. One patient (case 10) among the nine who underwent initial surgery without a lymphadenectomy developed a left iliac recurrence. She underwent a simple left pelvic lymphadenectomy followed by chemotherapy. Eight months later she developed a second recurrence in the right iliac nodes whose diagnosis was based on an elevated CA 125 level and a positive PET scan (only one suspicious site). She then underwent a right pelvic lymphadenectomy and para-aortic lymphadenectomy: 2 of 9 left pelvic nodes were positive and 18 para-aortic nodes were disease-free. She received six courses of platinum chemotherapy. She is currently disease-free, 6 months after the end of chemotherapy.

Four patients who relapsed underwent a lymphadenectomy during their initial surgical procedure. One of them (case 6) underwent a pelvic lymphadenectomy and had a recurrence 22 months later in the para-aortic area. Three others patients had a recurrence after a pelvic and para-aortic lymphadectomies performed during the initial surgical procedure.

Case 4. This patient underwent a complete pelvic and para-aortic lymphadenectomy; two positive nodes (of 37 removed) were found among the right common iliac and intercavo-aortic groups. Twenty-four months later she developed a recurrence in the right common iliac area.

Case 11. This patient initially underwent a complete pelvic and para-aortic lymphadenectomy (removal of 19 disease-free nodes). Postoperative chemotherapy was administered. Fifteen months later she developed a pelvic recurrence.

Case 7 is of particular interest. This patient underwent a complete pelvic and para-aortic lymphadenectomy initially. Eight of 28 nodes were metastatic (3 in the pelvic area and 5 in the para-aortic area). Six courses of chemotherapy were administered (platinum based plus paclitaxel). Six months later she developed a recurrence above the level of the left renal vessels. A complete surgical resection was performed (three bulky metastatic nodes were removed), followed by chemotherapy (six courses of topotecan). Thirty-four months later she had an elevated CA 125 level with an abnormal computed tomography (CT) scan. The PET scan depicted an isolated lesion on the splenic hilus. A new surgical procedure was performed (splenectomy). A single metastatic node (of four removed) was found inside the splenic hilus. Postoperative chemotherapy was administered (six courses of topotecan). The patient is currently disease-free, 6 months after the end of the last course of chemotherapy.

The histologic examination of the operative specimens of nodal recurrences confirmed that peritoneal cytology was negative in eight patients and positive in two (including the patient who had macroscopic disease on the peritoneum). No severe complications occurred during the second surgical procedure; in two cases, repair of wound dehiscence was associated with surgical resection of lymph nodes. One patient developed a postoperative complication (chylous ascites drained by a radio-guided puncture). Ten patients underwent postoperative chemotherapy, and radiation therapy was delivered to two (case 4: 40 Gy to the iliac area; case 9: 45 Gy to groin nodes); case 4 received both treatments.

Outcomes and Survival
The overall median duration of follow-up after the diagnosis of the nodal recurrence(s) was 50 (range, 13–158) months. Eight patients relapsed and four did not. The locations of the new recurrences were as follows: peritoneum (2), pleural cavity (1), spleen (1), and lymph nodes in 4 (iliac nodes in 2 patients, para-aortic nodes in 1, and lymph node metastasis to the splenic hilus in 1). Of the four patients who had a repeated nodal recurrence, three underwent a new surgical procedure with nodal resection (followed by chemotherapy in all patients). To date, three patients have died of the disease, three are alive with persistent disease, and six are alive and disease-free (including two patients who had a repeated recurrence in abdominal nodes that was treated by surgical resection). One patient (case 1) developed lethal progressive disease (pleural and supraclavicular nodes) 3 years after the first nodal recurrence. Adjuvant therapy was never discontinued in this patient. In nine patients, recurrent disease was diagnosed >12 months after the end of the initial treatment, and in three, within 12 months following the end of initial treatment (two of these latter patients are alive without evidence of disease and the third is alive with persistent disease).

Median overall survival from the date of the first surgical procedure was 114 (range, 43–172) months. Five-year overall survival from treatment of recurrent disease was 71% (CI, 41%–90%). Overall survival curves are given in Figure 1. Median overall survival cannot be calculated because, at the last follow-up, more than half of our population was still alive. Median survival without a second relapse was 44 (range, 8–158) months.



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  		FIG. 1. Overall survival among 12 patients.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the literature, numerous publications have focused on the prognosis following secondary cytoreductive surgery for EOC and/or on the results of surgical treatment of recurrent EOC.6–15 In most of these articles, recurrences were located in the intra-abdominal or extra-abdominal cavity, but the authors did not distinctly specify whether sites were nodal or extranodal.11,14 In other articles, recurrent nodal disease was included in larger series but mixed with other involved sites.8–10,13,15 Seemingly, a detailed assessment of the prognosis in the subgroup of patients with nodal recurrences alone has never been conducted, and to our knowledge, this is the first study to address the prognosis for patients with a nodal recurrence from EOC.

Our article raises several specific issues that differentiate patients with a nodal recurrence from patients with other sites of recurrence. The first issue concerns the impact of the initial surgical procedure on the risk of nodal recurrence. In a previous study, we assessed the results for 276 patients who underwent pelvic and para-aortic lymphadenectomies.4 Only three of these 276 patients (1.1%) developed a nodal metastasis alone (they are included in this current study), and 20 had a lymph node metastasis associated with metastatic lesions at other sites (such as the peritoneum, pleura, and deep parenchyma). In the present series, eight of the 10 patients with intra-abdominal relapses were not submitted to para-aortic and/or pelvic lymphadenectomies at the time of initial surgery. Even if the validity of a complete lymphadenectomy is still being debated, the above results suggest that this procedure could have a therapeutic value.

Among the four patients with recurrent disease and a previous history of lymphadenectomy, two had positive nodes at the time of the initial pelvic and para-aortic lymphadenectomies: one had a recurrence in an area that is not usually dissected during initial surgery (para-aortic nodes above the level of renal vessels) and the other one developed a para-aortic recurrence 2 years after the initial lymphadenectomy (with a positive para-aortic node). These two recurrences were probably unavoidable. The third patient developed a pelvic recurrence 15 months after the end of treatment, which included pelvic and para-aortic lymphadenectomies. However, during the surgical procedure, "only" 19 disease-free nodes were removed. As a small number of lymph nodes were removed, the recurrence could have been due to an incomplete surgical resection of nodes. The fourth patient underwent a pelvic lymphadenectomy alone during initial surgery outside our institution. She developed a recurrence in the para-aortic area. In the literature, the location of involved nodes varies in the literature: between 13% and 40% of positive nodes are found in the pelvic area and 15% to 40% in the para-aortic area.16–20 Thus, if a lymphadenectomy is performed in EOC, it should include pelvic and para-aortic nodes up to the level of the renal vein.

The second issue arising from our results concerns both the prognosis and treatment of nodal recurrences. We found that the survival of our patients with an a priori isolated nodal recurrence (with one or several nodes), was higher than that of patients with recurrences from EOC, whatever the site, treated at least by surgery. The 5-year survival rate was 28% among patients who underwent secondary cytoreductive surgery without macroscopic residual disease in the series reported by Eisenkhop et al.10 In a recent paper from China, only 10.43% of the patients with a residuum of <1 cm after secondary cytoreductive surgery were alive at 5 years.14 Finally, in the paper by Munkarah et al.,12 the median duration of survival after complete secondary cytoreductive surgery was 56.9 months. In the present series, 71% of the patients are alive and 50% of patients are alive without evidence of persistent disease. Such results seem to demonstrate that the prognosis for our patients with a nodal recurrence is relatively good, compared with that for patients with other sites of recurrence reported in the literature.

There is a bias, however, that limits the comparability of the different series, because our population comprised a selected group of patients (in principle, nodal metastasis alone, exclusion of patients with concomitant extranodal recurrence). The prognosis for such patients, with a solitary site of recurrence and absence of significant intraperitoneal disease, who were all treated with surgical resection, is therefore particularly high. It is noteworthy that in the literature, a statistically significant benefit was observed in the duration of survival among patients in whom all visible recurrent tumor tissue was completely removed at the time of secondary cytoreductive surgery.6,10,11

Because a complete surgical resection is feasible in most patients with a nodal recurrence, with the exception of patients with an intra-abdominal recurrence, survival should also be better among patients with a recurrence located exclusively in lymph nodes. Finally, we also know from the literature that patients with stage IIIC ovarian cancers based on dissemination of disease to retroperitoneal nodes have a better survival than patients with stage IIIC based on the presence of peritoneal disease. Indeed, Onda observed a much better 5-year survival rate among patients with stage III disease, based only on lymph node positivity, than among patients who were considered to have stage III disease, because they had intraperitoneal tumors (5-year survival: 84% vs. 26%; P = .042).21 These different elements could explain why we achieved such a "good" survival rate among our patients.

All our patients underwent a surgical procedure in order to remove metastatic nodes. Surgery was decided on the basis of the exclusion of patients without a solitary site of metastatic disease. Patients with several concomitant sites of metastasis (diagnosed before the surgical procedure) were treated with chemotherapy. The prognosis for such patients is poor. In the present series, surgical resection was followed in all patients (except in one patient with a single metastatic node) by adjuvant treatment (chemotherapy and/or radiation therapy). It is therefore difficult to clearly demonstrate that the optimal treatment in such patients is at least surgical resection, because there are no data in the literature on the survival of patients treated with chemotherapy alone for a solitary nodal recurrence. Perhaps, given the fact that none of our 12 patients had significant intraperitoneal disease, the long-term survival reported would have been achieved with exclusive chemotherapy (without surgical resection).

However, several studies in the literature do suggest that nodal metastases from EOC are chemoresistant lesions.16,17,22–27 Furthermore, a recent series reported by Kuhn et al.28 demonstrated that the survival of patients with a recurrence (whatever the site) was better among those who underwent secondary debulking surgery (followed by adjuvant therapy) than among patients treated with chemotherapy alone (median duration of survival: 38 versus 12 months; P < .0001). In the light of these findings, we think that surgical resection of lymph node metastasis should optimize survival in recurrent ovarian cancer. Even in cases of a second solitary nodal recurrence, surgical resection should be performed (if the patient’s medical status is good). In the present series, among the eight patients who developed a second relapse, three (cases 5, 7, and 10) underwent complete resection of the second recurrence, and two of them are still alive and disease-free 6 months after the end of adjuvant treatment for the second relapse.

In the present series, surgery was proposed to a group of patients with recurrent disease exclusively located in lymph node(s). Patient selection for surgery was based on imaging methods (CT and, more recently, PET). Patients with an extranodal recurrence diagnosed at imaging were treated with chemotherapy.

In the literature, the survival of relapsing patients is clearly related to the disease-free interval (DFI) after primary treatment, and survival after secondary surgery and chemotherapy has been previously described: patients with a DFI >12 months have a longer duration of survival than those with a shorter DFI.6,7,11 However, among the three patients with a DFI <12 months (one of them had a history of complete lymphadenectomy) in our series, no deaths are to be deplored and two are alive without evidence of persistent disease. Clearly, on the basis of this subgroup of patients with recurrent disease a priori, exclusively located in lymph nodes, the median duration of the DFI should not be taken into account when selecting patients for surgical resection.

The prognosis is good for this group of patients with an a priori isolated nodal recurrence from EOC treated by complete surgical resection followed by adjuvant therapy. Nodal recurrences are rare in patients with a previous history of complete para-aortic and pelvic lymphadenectomies. The DFI and the initial disease stage do not seem to influence outcomes. These findings argue in favor of surgical resection for an isolated EOC metastasis to lymph nodes. Definitive conclusions about present series are limited by the small number of cases reported and the presence of several biases (selected group of patient with a single site of metastasis). Larger series are needed in order to evaluated the survival of patients with isolated nodal recurrences from EOC treated by surgical resection.


   ACKNOWLEDGMENTS
 
The authors thank Lorna Saint Ange for editing the manuscript.


   FOOTNOTES
 
The prognosis for patients with a priori isolated nodal recurrence treated by at least surgical resection is relatively good in comparison with the prognosis reported in the literature for patients with recurrence located in other sites.

Received for publication November 7, 2003. Accepted for publication March 16, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Editorial: Secondary Cytoreductive Surgery for Isolated Nodal Recurrence of Ovarian Cancer
Ann. Surg. Oncol., July 1, 2004; 11(7): 639 - 640.
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