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10.1245/s10434-006-9048-2
Annals of Surgical Oncology 13:1717-1723 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Splenectomy During Secondary Cytoreduction for Ovarian Cancer Disease Recurrence: Surgical and Survival Data

Natalina Manci, MD1, Filippo Bellati, MD1, Ludovico Muzii, MD2, Marco Calcagno, MD1, Sagit Arbel Alon, MD1, Milena Pernice, MD1, Roberto Angioli, MD2 and Pierluigi Bendetti Panici, MD1

1 Department of Gynecology and Obstetrics, University of Rome "La Sapienza", V.le Regina Elena, 324, 001161 Rome, Italy
2 Department of Obstetrics and Gynecology, Campus Bio Medico University of Rome, Rome, Italy

Correspondence: Address correspondence and reprint requests to: Natalina Manci, MD; E-mail: natalina.manci{at}uniroma1.it.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
Background: Ovarian cancer disease recurs predominantly in the abdomen, with the spleen usually involved as part of a vast spread of upper-abdominal disease or, less frequently, as an isolated site of disease recurrence. Very few reports are available in the literature on the outcome of patients subjected to splenectomy during secondary cytoreduction. The aim of this study was to identify prognostic factors and to review surgical and clinical data in order to identify those patients who would benefit the most from splenectomy during secondary cytoreduction.

Methods: This was a retrospective review of platinum-sensitive recurrent epithelial ovarian cancer patients who underwent splenectomy as part of secondary cytoreduction. Surgical and survival data were recorded.

Results: Twenty-four patients were identified. Multiple site disease recurrence was observed in 15 patients. The spleen was involved at the hilus in 12 patients; surface and intraparenchymal metastases were equally present. Optimal cytoreduction was achieved in all patients. At a median follow-up of 30 months, median progression-free and overall survival from the time of secondary surgery were 34 and 56 months, respectively. Overall survival was significantly correlated to residual disease at secondary surgery, disease-free survival, consolidation chemotherapy, and type of adjuvant therapy.

Conclusions: Splenectomy as part of secondary cytoreduction is a feasible and safe procedure. Secondary cytoreduction in selected groups of patients is confirmed to be associated with high long-term survival rates even when aggressive surgery of the upper abdomen is required.

Key Words: Ovarian cancer recurrence • Secondary cytoreduction • Splenectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
Ovarian cancer is the primary cause of death for gynecologic malignancies in industrialized countries.1 First-line treatment includes cytoreductive surgery and platinum-based chemotherapy.2,3 More than one-half of the patients treated with first-line chemotherapy achieve a clinical complete response, but only a one-quarter will benefit from long-term disease remission.4 To date, no unanimous consensus has been reached on the strategy that should be adopted in recurrent patients. Possible strategies include second-line chemotherapy5 or secondary cytoreduction.6 Secondary cytoreduction frequently requires aggressive surgical procedures that are inevitably associated with significant intra- and postoperative morbidities. In the paucity of literature data, physicians are required to carefully tailor treatment strategies on the basis of patients’ characteristics and prognostic factors.

The recurrence of ovarian cancer disease involves the abdomen in most cases.7 The spleen is usually involved as part of a vast upper-abdominal disease spread8,9 or, less frequently, as isolated disease recurrence site.10,11 There are very few reports in the literature on the outcome of patients subjected to splenectomy during secondary cytoreduction, and most of these consist of case reports or small case series. The purpose of this study was to identify prognostic factors and to review surgical and clinical data in order to be able to select patients who would most benefit from splenectomy during secondary cytoreduction.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 CONCLUSIONS
 REFERENCES
 
Patients
This was a retrospective review of the charts of 106 patients scheduled to undergo secondary cyto-reduction between 1995 and 2004. All of the patients had been personally treated by the senior author (PBP). Twenty-two patients (21%) were subjected only to diagnostic laparoscopy without any further attempt at cytoreduction; the remaining patients charts were reviewed for inclusion criteria. Twenty-four patients (29%) who underwent splenectomy were identified. Criteria for inclusion were the following: invasive epithelial ovarian cancer (borderline tumors were excluded), cytoreductive surgery and platinum-based chemotherapy, disease-free interval (DFI) of more than 6 months, and histologically documented disease involvement of the spleen removed during secondary cytoreduction (patients undergoing splenectomy for intraoperative spleen trauma were excluded). Information on the patients and tumor characteristics, therapeutic strategy, diagnostic work-up leading to diagnosis of recurrence, surgical and survival data was retrieved. Optimal cytoreduction was defined as a macroscopic residual tumor (RT) smaller than 0.5 cm in the abdominal cavity. Postoperative complications were defined as adverse events occurring within 4 postoperative weeks. DFI was defined as the interval between the end of adjuvant platinum-based chemotherapy (not including consolidation chemotherapy) and pathological diagnosis of recurrence. Overall survival (OS) was defined as the interval between secondary surgery and the last follow-up or death of the patient. Progression free survival (PFS) was defined as the interval between secondary surgery and the last follow-up or disease progression of the patient. The end-point of the follow-up period was November 2004.

Statistical Analysis
Parametric tests were used after having evaluated the normal distribution of the data to be analyzed. Student’s t-test and the Mann-Whitney U-test were used for comparing the parametric and nonpara-metric numerical data, respectively, whereas the Fisher’s exact test and the chi-squared test were used for categorical data. Survival was calculated using the life tables’ method of Kaplan and Meier, and comparisons were made using the log-rank and Breslow-Gehan-Wilcoxon tests. A P value < 0.05 was considered to be significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
CONCLUSIONS
 REFERENCES
 
Patients’ Characteristics
Twenty-four patients were identified. Twenty-one patients (87.5%) were initially diagnosed with FIGO stage III disease, whereas the remaining three (12.5%) were affected by stage IV disease (one patient with positive cytology of pleural effusion, and two patients with central liver metastasis). Histology was serous, mucinous, endometrioid, and undifferentiated in 14 (58%), two (8%), two (8%), and six (26%) cases respectively. The tumor grade was 1 in two patients (8%), 2 in three patients (13%), 3 in 17 patients (71%), and unspecified in two patients (8%). Twenty-two patients (92%) were subjected to primary cytoreduction followed by six cycles of adjuvant platinum-based chemotherapy, whereas the remaining two patients (8%) received prior chemotherapy before surgical cytoreduction. At primary cytoreduction (or interval debulking surgery) all patients identified achieved optimal cytoreduction (RT ≤ 0.5 cm) and 11 patients (46%) had no residual disease. In 21 patients (88%) a complete clinical response was confirmed by second-look surgery. Thirteen patients (54%) were treated with consolidation chemotherapy with 60 mg/m2 intraperitoneal paclitaxel weekly for 16 weeks. Median DFI was 26 months (range: 6–119). Patients’ characteristics at secondary surgery are listed in Table 1Go. The median age of the patient cohort was 54 years (range: 27–69). The first sign that led to the diagnosis of recurrence was increasing levels of CA-125 during follow-up (15 patients, 63%) and a positive computed tomography (CT)/magnetic resonance (MR) image (and normal CA-125) (eight patients, 33%). One patient (4%) who was involved in an internal trial was diagnosed on the basis of a positive positron emission tomography (PET) scan, in the presence of normal CA-125 values and a negative CT scan (Fig. 1Go). Seven patients (29%) had a preoperative diagnosis of multiple lesions. In none of the patients was carcinomatosis suspected preoperatively.


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  		TABLE 1. Preoperative characteristics at secondary cytoreduction
 

Figure 1
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  		FIG. 1. 18F-Fluoro-deoxyglucose positron emission tomography (PET) showing an increased uptake in the splenic region.

 
Surgical Findings
All patients were subjected to diagnostic laparoscopy before laparotomy. Surgical findings and operative data are reported in Table 2Go. At surgery, 15 patients (62%) were found to have more than a single lesion. The largest spleen lesion was at the hilus (12 patients, 50%). Intraparenchymal and superficial spleen involvement were equally present in six patients (25%). Intraparenchymal lesions were always found as a solitary lesion, whereas hilar and superficial spleen involvements were mostly found as part of multiple-site disease recurrence. Carcinomatosis was present in most patients with multiple lesions (11 cases, 73%). The most frequently encountered extrasplenic lesions were on the bowel and on the pelvic/abdominal wall. Major associated procedures, in addition to splenectomy, were carried out in 16 patients (67%) and included: extensive stripping (diaphragmatic and bilaterally paracolic gutter) or argon beam coagulation (11 patients, 46%), large bowel resection (5 patients, 21%), small bowel resection (two patients, 8%), distal pancreatectomy (four patients, 17%), partial hepatectomy (two patients, 8%), lymphadenectomy (two patients, 8%), and partial gastrectomy (one patient, 4%). One bowel resection and all pancreatectomies were performed for technical surgical reasons or to achieve optimal debulking in the spleen hilar region and not for direct organ involvement (Fig. 2Go). Median operative time was 155 minutes (range: 50–480). Median estimated blood loss was 610 ml (range: 320–1800 ml). As expected, both operative time and estimated blood loss were significantly greater in patients affected by multiple lesions than in patients with solitary disease recurrence (P = 0.008, P = 0.004, respectively). Five patients (21%) required blood transfusions and five patients (21%) had intraoperative hemorrhage with blood loss of more than 1000 ml (range: 1100–1800). No other major intraoperative complications were reported. Major postoperative complications were early postoperative small bowel obstruction (one patient, 4%), pulmonary embolism (one patient, 4%), and a pancreatic fistula (one patient, 4%). All patients were treated conservatively and no reoperation was performed. Median postoperative hospital stay was 6 days (range: 3–13 days).


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  		TABLE 2. Comparison of operative and perioperative data between isolated and multiple lesions
 

Figure 2
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  		FIG. 2. Operative specimen including: the spleen (A), the duodenum (B), the pancreatic tail (C), and the left colonic flexure (D).

 
All patients received vaccination for S. pneumoniae, H. influentiale, and N. meningitides, and no episode of sepsis was registered during the follow-up period.

Splenectomy was performed at the end of the surgical procedure or after having assessed the possibility of achieving optimal cytoreduction and, as expected, all patients benefited from optimal cytoreduction; in addition, 16 patients (67%) had no macroscopic residual disease at the end of secondary surgery. All patients received postoperative intravenous chemotherapy (Table 3Go).


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  		TABLE 3. Chemotherapy regimen after secondary cyto-reduction
 
Survival Data
Of the 24 patients identified (median follow-up: 30 months; range: 5–100 months), 13 patients were still alive with no evidence of disease after a median time of 33 months (range: 9–100 months), four patients were alive with clinical evidence of disease after a median time of 32 months (range: 22–45 months), and seven patients died of disease after a median time of 21 months (range: 5–56 months). Median progression-free and overall survival from secondary surgery were 34 and 56 months, respectively (Fig. 3Go).


Figure 3
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  		FIG. 3. Kaplan and Meier survival curves from secondary surgery.

 
All six patients with isolated intraparenchymal spleen recurrence were alive and disease-free with the writing of this article (median follow-up: 27.5, range: 11–100 months).

Survival rate was significantly longer in patients who were completely cytoreduced (RT = 0) than in those who were not (estimated 3-year OS: 91 vs. 62.5%, P = 0.002). Moreover, survival rate was significantly related to DFI (>12 months vs. ≤12 months; estimated 3-year OS: 100 vs. 50%, P = 0.002), consolidation chemotherapy (no consolidation vs. intraperitoneal paclitaxel; estimated 3-year OS: 100 vs. 65%, P = 0.003), and chemotherapy after splenectomy (platinum-based vs. non-platinum based; estimated 3-year OS: 100 vs. 51%, P = 0.03). Age, residual disease at primary surgery, CA-125, number of lesions, and carcinomatosis did not alter the survival rates significantly.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
REFERENCES
 
Splenectomy during secondary cytoreduction appears to be a feasible and safe procedure and may be associated with long-term survival. It should be noted that the patients analyzed in this report represent a subgroup of patients with a long disease-free interval and chemotherapy-responding tumors and who had achieved optimal residual disease at primary surgery. In addition, splenectomy during secondary surgery was performed only in patients who were judged to be optimally cytoreducible at laparoscopy.

As expected, surgical difficulty, using operative time and estimated blood loss as surrogate markers, was significantly greater for patients with multiple lesions than with patients affected by solitary lesions. The severe perioperative complication rate was low in both groups. Unfortunately, a high proportion (8/17, 47%) of those patients with preoperative diagnosis of solitary lesions were found to have multiple lesions and, therefore, it was not possible to determine surgical difficulty preoperatively; this development highlights the necessity for such patients to be treated in referral oncology centers.

Survival rate was affected by residual tumor at secondary cytoreduction (0 vs. 0.5 cm), DFI (<12 months vs. >12 months), consolidation chemotherapy (no consolidation vs. intraperitoneal paclitaxel), and adjuvant chemotherapy after splenectomy (platinum-based vs. non-platinum-based chemotherapy). The prognostic relevance of RT,6,12 DFI,13 and type of chemotherapy14 has already been described in previous reports. Consolidation chemotherapy has been demonstrated to improve progression-free survival in phase III trials.15 It is possible that the negative association between consolidation chemotherapy and survival in the present report was caused by a physician bias that resulted, at the end of standard adjuvant chemotherapy, in only patients with negative prognostic factors (i.e., residual tumor, his-totype, tumor grading) being treated with intraperitoneal paclitaxel. In the present series, however, we were unable to identify such factors, although the retrospective nature of the trial does not allow us to exclude completely this hypothesis. An alternative hypothesis is that micrometastases that persist after intraperitoneal paclitaxel are biologically more aggressive.

Spleen involvement in ovarian cancer has been reported to be as high as 20%16. The spleen can be involved either as a solitary lesion,10,11 or, more frequently, as part of extensive carcinomatosis of the upper abdomen. Only a small number of trials9,11,17–31 have addressed the issue of splenectomy during ovarian cancer surgery, and only a few of these have included patients being subjected to secondary cytoreduction.9,17,20,23,25,27,30

Deppe et al.17 reported the first case of splenectomy during secondary cytoreduction in a patient who had benefited from a 5-year DFI. This patient was disease free after 1 year of follow-up; however, no further information is available on the longer follow-up. Morris et al.20 analyzed the indications and complications associated with splenectomy in 45 patients. In their study, 24 patients underwent splenectomy during ovarian cancer cytoreduction, 15 of whom as secondary cytoreduction. The overall complication rate was 29% with one postoperative death.

Nicklin et al.23 reported results obtained in 18 patients who had been subjected to splenectomy during surgical cytoreduction, with 11, one, one, and five patients undergoing a splenectomy during primary cytoreduction, interval debulking surgery, second-look laparotomy, and secondary cytoreduction, respectively. Four patients of the latter group were affected by recurrent ovarian cancer, whereas the remaining patient was affected by fallopian tube cancer. Splenectomy was performed in 13 cases for parenchymal, hilar, or capsular disease. Residual disease was ≤5 mm in ten patients. Intraoperative complications included pancreatic tail lesions in four cases. The mean operating time was 368 minutes (range: 180–560 minutes), and mean estimated blood loss was 1578 (400–2800) ml. Of the 18 patients undergoing this procedure, 11 had died of disease at a median time of 12.0 months postoperatively (range: 5–59.5 months); five patients were alive with disease at a median time of 8 months postoperatively (range: 2–16 months); two patients were alive with no clinical evidence of disease at 2.5 months of follow-up. When the patients of our series are compared to those of Nicklin et al., our achievement of optimal residual disease and survival data would appear to be superior. In addition, the surgical time and blood loss reported by Nickin et al. appear to be higher (mean operative time and mean operative blood loss in the present series were 180 ± 108 minutes and 735 ± 401ml, respectively). This large discrepancy between our results and those reported by Nicklin et al. is likely due to the completely different study cohorts in these studies; in fact, only five out of the 18 cases were secondary cytoreduction in Nicklin et al.’ s study.

Scarabelli et al.25 evaluated 40 patients affected by ovarian cancer. Twenty-six patients underwent splenectomy during secondary cytoreduction, but only 22 actually had histologically confirmed spleen disease involvement. Nineteen patients (73.1%) had recurrent disease after a DFI of more than 12 months, whereas the remaining seven (26.9%) had recurrent disease while receiving first-line chemotherapy. At the end of surgery 15 (57.7%) patients had no residual intra-peritoneal disease, whereas the remaining 11 (42.3%) had intraperitoneal residual disease (<2 cm). The median operating time in all 40 patients was 330 minutes, and the median number of blood units transfused was three. The estimated 2-year survival rate for patients with no residual disease and <2 cm intraperitoneal residual disease was 78 and 24%, respectively, and the estimated 3-year survival rate was 0% for all patients. The estimated median survival rate for patients with no residual disease and < 2 cm intraperitoneal residual disease was 27 and 16 months, respectively. The study conducted by Scarabelli et al. was carried out in patients undergoing either primary or secondary cytoreduction. In the latter group, surgical outcome was not significantly lower than that reported in this series (RT = 0, 15/ 26, 58% vs. 16/24, 67%, respectively). The median operating time and median blood units transfused for all 40 patients were higher. It is likely that the figures in Scarabelli et al.’ s investigation reflect their inclusion in the analysis of patients undergoing primary cytoreduction. Compared to Scarabelli, the present study obtained higher survival rates, which again is probably due to different patient selection criteria.

Lee et al. (27) reported the 10-year experiences of surgeons at a large teaching hospital carrying out splenectomy. Twenty-three patients were subjected to splenectomy for ovarian cancer, 18 of whom were treated for a recurrent disease. Mean time to recurrence from primary cytoreduction for 17 patients was 3.9 years (range: 1–9 years). Mean survival for all 23 patients was 22.9 months (range: 1–72 months). During the 10 years (1990–1999) covered by the study, these authors reported a significant increase in the number of splenectomies for cancer metastases carried out within the institution and, in particular, an increase in parenchymal ovarian metastases. A possible explanation suggested by the authors was the increasing tendency of physicians to carry out intra-peritoneal chemotherapy with direct action on the spleen capsule. In the present series, DFI appears to be shorter and OS appears to be longer than those reported by Lee et al. It is not possible to compare these two series since the objectives of the paper reported by Lee et al. were different from those of the present one. We believe that an alternative hypothesis to justify the increase in incidence of splenectomy in the last decade may be the increase in number of physicians that adopt secondary cytoreduction as a therapeutic strategy.

Chen et al.9 reported 22 patients undergoing splenectomy as part of secondary cytoreduction. Only one-half of the patients were platinum-sensitive. Eight patients (36%) had disease confined to one quadrant, whereas in the remaining 14 (64%) patients, three or four abdominal quadrants were involved. The pattern of spleen involvement was on the spleen surface in 15 (68%) patients, on the parenchyma in 13 (59%) patients, and on the hilus in 15 (68%) patients. Associated procedures were mainly omentectomy and gastrointestinal resection. Optimal cytoreduction was achieved in 19 (86%) patients, and 14 (64%) were cytoreduced to no visible disease. Six patients (29%) suffered from major postoperative morbidity. The median survival interval was 41 months. In the series of Chen et al., the mean operative time, mean blood loss, and proportion of patients cytoreduced to microscopic disease were comparable to those of the present study, although median survival was shorter in the former (44 vs. 56 months), possibly due to the inclusion of non-platinum-sensitive patients.

Chi et al.30 have recently proposed an innovative surgical approach reporting the results obtained in five patients undergoing splenectomy for secondary cytoreduction. Splenectomy was performed using hand-assisted laparoscopy or laparoscopy in three and two cases, respectively. Mean operative time and mean blood loss was 258 ± 64 minutes and 150 ± 117 ml, respectively. Only one patient was subjected to blood transfusion. All patients (with the exception of one who was subjected to surgery for a second look) achieved optimal cytoreduction. The patients were discharged from hospital at a median time of 4 days (range: 3–5 days) postoperatively. The survival status of the two patients who had benefited from a long DFI before being found with malignant lesions showed no evidence of disease at 2 and 84 months, respectively.

Although the study of Chi et al. is based on a small number of patients, their results appear to be better than those obtained in our series even when analyzing patients affected by isolated splenic lesions. In the present series, the mean operative time and mean blood loss were 108 ± 40 minutes and 526 ± 184 ml, respectively. The median postoperative stay was 6 days (4–9 days). It would seem that the increase in surgical time obtained in the series reported by Chi et al. is a minor disadvantage when compared with the significant decrease in blood loss and postoperative stay. If, as the authors stated, these results will be confirmed in larger series, it is hopeful that laparos-copy or hand-assisted laparoscopy will become standard surgery carried out in such patients.

In conclusion, splenectomy during secondary cytoreduction is a feasible and safe procedure. This analysis confirms that patients affected by isolated intraparenchymal lesions benefit from long-term disease-free survival. Selected patients may benefit from secondary cytoreduction even when aggressive surgery of the upper abdomen is required.

Received for publication August 26, 2005. Accepted for publication February 15, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 

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