Annals of Oncology Advance Access originally published online on May 11, 2007
Annals of Oncology 2007 18(12):1943-1950; doi:10.1093/annonc/mdm137
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© 2007 European Society for Medical Oncology
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Systematic review of cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy for treatment of peritoneal carcinomatosis in primary and recurrent ovarian cancer
1 Peritoneal Surface Malignancy Program, Washington Cancer Institute, Washington DC
2 Department of Women's Services, Washington Hospital Center, Washington DC, USA
* Correspondence to: Dr P. H. Sugarbaker, Peritoneal Surface Malignancy Program, 106 Irving Street, NW, Suite 3900N, Washington DC, USA 20010. Tel: +1-202-877-3908; Fax: +1-202-877-8602; E-mail: paul.sugarbaker{at}medstar.net
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Abstract |
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The aim of this systematic review is to critically evaluate cytoreductive surgery combined with heated intraoperative intraperitoneal chemotherapy in the treatment of ovarian cancer. A systematic review of all manuscripts published in the English literature that met predetermined inclusion criteria was carried out. Data concerning cytoreductive surgery, method and agents for administration of heated intraoperative intraperitoneal chemotherapy, morbidity, mortality, hospital stay and survival were extracted, critically reviewed and tabulated. Fourteen studies were analyzed. A wide variety of drug doses, methods of intraperitoneal chemotherapy administration and volume of chemotherapy solution were used. Seven studies showed that patients with complete cytoreduction had the greatest benefit. The median overall survival for primary and recurrent disease ranged from 22 to 54 months and the median disease-free survival from 10 to 26 months. The rates of significant morbidity associated with this combined treatment were low, ranging from 5% to 36%. The median mortality was 3% (range 0%–10%). Cytoreductive surgery combined with heated intraoperative intraperitoneal chemotherapy is a treatment option for patients with ovarian cancer that is worthy of further investigation. Selection criteria for patients most likely to benefit need to be defined.
Key words: cytoreductive surgery, heat, hyperthermia, intraperitoneal chemotherapy, ovarian cancer
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Ovarian cancer is the fifth leading cause of cancer-related deaths among females in the United States with 15 310 deaths projected in 2006.The majority of cases are diagnosed at an advanced stage and despite a 60%–80% [1] response rate to platinum-based systemic chemotherapy, the prognosis remains poor due to a high rate of recurrence.
Epithelial ovarian cancer has a marked propensity for peritoneal spread, which makes it suitable for aggressive local regional therapies. Consequently, the combination of intravenous and intraperitoneal route of administration for chemotherapeutic agents in ovarian cancer has been studied in three large randomized trials [2–4]. The most recent study [2] demonstrated that bidirectional chemotherapy using intravenous paclitaxel plus intraperitoneal cisplatin and paclitaxel significantly improved survival in patients with optimally debulked stage III disease. Encouraging results with bidirectional chemotherapy from Zylberberg et al. [5] were obtained by intraperitoneal cisplatin–paclitaxel and intravenous ifosfomide. Despite convincing data, this treatment modality is still not universally accepted due to the increased rate of complications associated with intraperitoneal drug delivery and the lack of familiarity with the technique among clinicians.
Cytoreductive surgery combined with heated intraoperative intraperitoneal chemotherapy is a comprehensive treatment modality directed at the whole abdomen and pelvis that has shown efficacy in the treatment of malignancies with peritoneal dissemination [6]. The use of intraperitoneal chemotherapy at the time of surgery and/or in the immediate postoperative period facilitates uniform drug delivery and may avoid some of the complications of prolonged peritoneal access. The addition of heat augments the cytotoxic effect of many chemotherapeutic agents by increasing cell membrane permeability [7].
The aim of this systematic review is to critically evaluate the morbidity, mortality and survival benefit of cytoreductive surgery combined with heated intraoperative intraperitoneal chemotherapy for ovarian cancer. From this systematic review, the rationale for integration of this combined treatment into the management of ovarian cancer should become apparent.
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patients and methods |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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A Medline search of all English language articles with the headings and key words ‘ovarian carcinoma’, ‘ovarian cancer’, ‘hyperthermia’, ‘chemohyperthermia’, ‘intraperitoneal’, ‘chemotherapy’ and ‘chemoperfusion’ was carried out. The key words were used in all possible combinations to retrieve the maximal number of articles. The articles were then screened for the presence of the following inclusion criteria: patients with advanced primary (International Federation of Gynecology and Obstetrics stage III and IV), persistent or recurrent ovarian cancer and intraperitoneal chemotherapy given intraoperatively and/or in the immediate postoperative period (1–5 days) following an attempt at maximal surgical cytoreduction and analysis of morbidity, mortality, survival or quality of life. Studies that reported results of treatment with this abdominopelvic modality for different malignancies were included, if data for ovarian cancer were reported and analyzed separately for at least one variable. All types of study designs were included. The bibliography of all selected articles was hand searched to identify additional articles that met our inclusion criteria.
Studies that reported only pharmacological data were excluded. Reports on low-grade (borderline) tumors were excluded, as were reports on appendiceal malignancies with ovarian spread. In cases where multiple publications were available with increasing number of patients or longer follow-up from the same group, only the most recent update was included. The formal published version of each article that met inclusion criteria was then analyzed by two authors and the following data were extracted: type of study design, year of publication, number of patients, criteria used to define maximal cytoreduction and the percentage of patients successfully cytoreduced, prognostic factors analyzed in association with outcomes, method used for intraperitoneal chemotherapy administration, chemotherapy agents and doses given, survival, morbidity and mortality. A meta-analysis was not appropriate due to the heterogeneity of patient populations and the differences of the treatment regimens among the studies [8].
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results |
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characteristics of the studies
Twelve publications that met inclusion criteria were identified after review of 85 abstracts retrieved from the Medline search. Two additional relevant publications were identified from the bibliography of these articles. Most of the included studies analyzed patients with primary and recurrent cancer together. There was a single nonrandomized prospective study while all the others were retrospective analyses. Five of the 13 retrospective studies stated the inclusion criteria for patients' entry into their treatment protocol. Eleven studies [9–19] focused on ovarian cancer patients with a mean of 24.7 patients per study (range 5–57). Three studies [20–22] reported results of different types of cancer treated with cytoreduction and heated intraoperative intraperitoneal chemotherapy but analyzed the subset of patients with ovarian cancer separately. The mean number of patients in these subsets was 8 (range 6–12). The characteristics of the included studies, with bullets indicating all the topics addressed by the authors, are shown in Table 1.
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cytoreductive surgery
In ten studies [9–17, 19], the definition of optimal or complete cytoreduction was provided. Some of the studies [10–12, 14, 20] used the completeness of cytoreduction (CCR) classification previously described by Sugarbaker [23]. In this classification, CCR-0 indicates no visible evidence of disease after cytoreduction, CCR-1 indicates residual tumors
2.5 mm in diameter, CCR-2 indicates tumors between 2.5 mm and 2.5 cm and CCR-3 indicates tumors >2.5 cm in diameter or a confluence of tumor nodules. CCR-0 and CCR-1 are considered complete cytoreductions. The rate of complete cytoreduction according to Sugarbaker's classification in the studies that used it varied as follows: Raspagliesi [10] achieved a 100% rate, Reichman [11] 85%, Zanon [14] 77% and Look [12] 57%. Other authors used different definitions of adequate cytoreduction. Piso [13] considered a cytoreduction complete if tumor residuals were <2 mm and achieved it in nine of 19 patients, DeBree [17] and van der Vange [19] reduced tumor to <5 mm in 15 of 19 patients and five of five patients, respectively, Ryu [15] and Rufian [9] reported a tumor reduction to <1 cm in 48 of 57 and 28 of 30 patients, respectively, while Chatzigeorgiou [16] achieved a cytoreduction to <1.5 cm in 12 of 20 patients. Three studies [18, 21, 22] did not clearly report the results on completeness of cytoreduction while Hadi [20] reported the results for all cancer types together.
Several studies emphasized the relationship between complete cytoreduction and improved outcomes. Look [12] found that a complete cytoreduction (residual disease of <2.5 mm) was associated with improved median survival (55.9 versus 8 months, P = 0.037) in multivariate analysis. Similarly, Raspagliesi [10] found that CCR-score in addition to the World Health Organization performance status and the extent of the carcinomatosis influenced outcome. Rufian [9] showed that completeness of cytoreduction and lymph node involvement were factors predictive of survival in multivariate analysis. Ryu [15] reported that a cytoreduction to <1 cm conferred a significantly better disease-free interval (hazard ratio 0.355, P = 0.0005) and overall survival (hazard ratio 0.38, P = 0.003). Piso [13] reported that a resection to <2 mm residual tumor showed a trend toward better survival without reaching statistical significance. Reichman [11] demonstrated that all the patients with a cytoreduction to no visible disease in their study were alive at the time of publication while the incompletely resected patients had an overall survival of 20 months (P = 0.03). Table 2 presents the information regarding cytoreductive surgery in these manuscripts.
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heated intraoperative intraperitoneal chemotherapy and early postoperative intraperitoneal chemotherapy
Cytoreductive surgery was combined with intraperitoneal chemotherapy utilizing heat in the operating room and/or at normal temperature in the early postoperative period; these treatments may be referred to as perioperative intraperitoneal chemotherapy.
Two different methods of administration of the heated intraoperative intraperitoneal chemotherapy were described in these studies. The open technique was used in seven studies [9, 11–13, 19–21]. This method involves the instillation of the chemotherapy solution into the open abdominal cavity with manual stirring to assure even distribution of the chemotherapy agents and heat. In the closed technique, the abdominal fascia is either temporarily or permanently closed after completion of the surgery including all the anastomoses and the chemotherapy solution circulated into the cavity through several catheters with the aid of a pump. Technical problems were reported in only one study [14] consisting of misperfusion into the abdominal wall (one patient) or the pleural cavity (one patient). Both were treated by early termination of the heated intraperitoneal chemotherapy treatment.
A variety of different chemotherapy agents and doses were employed. Most regimens described in the studies included cisplatin (doses of 50–150 mg/m2) with or without the use of thiosulfate [13] or amifostine [15] for renal protection. Intraperitoneal chemotherapy given in the immediate postoperative period was used in four studies [11, 12, 17, 19]. Table 3 outlines the technique, chemotherapy agents and doses reported in the studies reviewed.
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survival
The median follow-up in the studies ranged from 13.7 to 30 months. Five studies did not specify the duration of follow-up [9, 16, 18, 20, 21] while Ryu [15] (46.7 ± 23.8 months for the heated intraoperative intraperitoneal chemotherapy group) and Kober [22] (9.2 months) expressed it as a mean.
The survival as reported in the studies is shown in Table 4.
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morbidity and mortality
All of the studies presented morbidity and/or mortality data. There were six studies that had no deaths related to this treatment [9–12, 19, 21], four studies [13, 14, 18, 22] had one death (mortality 3.3%–9%) and three studies [15–17] had two deaths (3.3%–10% mortality). Hadi [20] reported a total of four deaths (5.6%) in their series of 71 patients (all malignancies combined); two of those were attributed to mitomycin C administered intravenously which was subsequently removed from the protocol.
Eight studies [10, 12–15, 17, 21, 22] reported their significant morbidity (complications requiring return to the surgical intensive care unit, an invasive procedure or return to the operating room). These serious complications were reported separate from the total morbidity with a range of 5%–36%. Four studies [9, 18–20] reported their total morbidity with a range of 45%–60%, including minor complications. The most significant complications and their rates in different studies as well as mean duration of hospital stay and mortality are shown in Table 5.
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discussion |
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In planning future clinical research in ovarian cancer, one wonders how the data from successful clinical trials [2–4] on intraperitoneal chemotherapy for ovarian cancer will be utilized. It seems unlikely that the practicing oncologist will decide that placement of an intraperitoneal port is indicated in every patient. Also, the optimal dosing of long-term intraperitoneal cisplatin and paclitaxel is still to be clarified. Despite the fact that the majority of patients fail current treatment schedule with debulking surgery and systemic chemotherapy, no standard of care has emerged regarding secondary cytoreduction for recurrent disease. This systematic review indicates that future clinical research in ovarian cancer should include the evaluation of heated intraoperative intraperitoneal chemotherapy. This approach would ensure that every patient has at least one cycle of this new route for chemotherapy administration unless they were left with bulky residual disease after cytoreduction.
The most recent trial [2] using long-term intraperitoneal chemotherapy showed improved survival in the group of patients treated with bidirectional (intraperitoneal and intravenous) chemotherapy (65.6 versus 49.7 months). It also showed that this group of patients experienced a higher number of complications and a lower quality of life. Approximately half the patients who were randomly assigned to receive intraperitoneal chemotherapy in this study received three or less cycles by the intraperitoneal route instead of the planned six cycles; nevertheless, they had a significantly better survival. It is possible that the benefits of intraperitoneal chemotherapy will be greater if the intraperitoneal chemotherapy is administered only in the perioperative period. The administration of intraperitoneal chemotherapy in the perioperative period may become a way to successfully overcome the major impediments that prevented the intraperitoneal delivery of chemotherapeutics to become widely accepted. Perioperative intraperitoneal chemotherapy has several advantages over intraperitoneal treatments administered over prolonged periods of time. It allows the delivery of drugs combined with heat. It is delivered immediately after optimal surgical reduction and complete lysis of adhesions allowing for improved drug distribution. Perhaps, most important from a patient perspective, it avoids the complications associated with placement and maintenance of a peritoneal access device and therefore provides full compliance.
The rationale for an aggressive approach to the treatment of advanced stage and recurrent ovarian cancer is that the disease tends to recur in large volume in the peritoneal cavity. It is possible that treatments found to be beneficial in other disease states with a similar pattern of spread may find application in ovarian cancer. Cytoreductive surgery combined with heated intraoperative intraperitoneal chemotherapy has recently received considerable attention based on the success of treatment of pseudomyxoma peritonei and diffuse malignant peritoneal mesothelioma [23–26]. Treatment of carcinomatosis from colorectal cancer using this technique has been studied in a prospective randomized trial. This level I evidence showed a clear survival advantage for the group treated with cytoreductive surgery plus heated intraoperative intraperitoneal chemotherapy compared with palliative surgery and systemic chemotherapy [27]. The evidence presented in this systematic review indicates that cytoreductive surgery and heated intraoperative intraperitoneal surgery are a viable option in the management of ovarian cancer.
The benefit of surgical cytoreduction in ovarian cancer has been studied in a multitude of retrospective studies. Several meta-analyses [28, 29] showed a correlation between the percentage of maximal cytoreduction and outcome. Secondary cytoreduction for recurrent or persistent disease appears also to confer a survival advantage over systemic chemotherapy [30, 31] in some studies. The definition of optimal cytoreduction, however, is still controversial and often differs among studies. The experience with aggressive cytoreductive surgery and heated intraoperative chemotherapy in other peritoneal malignancies shows that a more restrictive definition of optimal cytoreductive surgery (<2.5 mm) has the best correlation with outcome. It has been shown in multiple models that the penetration of intraperitoneal chemotherapeutics into tumor nodules is limited to 0.5–2 mm [7] and therefore it is unlikely that substantial benefit from a local-regional treatment can be achieved with larger residual tumor nodules. Some authors have indicated that optimal cytoreduction in patients with recurrent ovarian cancer requires no visible residual disease [32]. For primary cancer, residual nodules of 1 cm or 0.5 mm may be acceptable. Indeed, the results of the studies in this review indicate that aggressive cytoreduction and its associated morbidity and mortality is probably not justified in cases where complete cytoreduction cannot be achieved since these patients have a median survival of only 8 months [12]. However, as shown in Table 2, optimal cytoreduction conferred an improved survival in seven of the nine studies that analyzed this variable.
This systematic review clearly illustrates the great variety of chemotherapy agents and doses used for intraoperative intraperitoneal chemotherapy. Also, both an open abdomen and a closed abdomen methods are used. Current data indicates that vigorous agitation of the intraperitoneal fluid increases the contact area of the peritoneum and may indicate that the open technique is superior to the closed method [33]. Technical problems such as spillage of the solution can usually be avoided if precautions are taken. Experiments in animals have also shown that prolonged dwelling time (24 h) of the chemotherapy solutions provide improved penetration and this principle can be utilized with early postoperative intraperitoneal chemotherapy [33]. Available pharmacological and animal data should be used to guide decisions regarding optimal choices for intraperitoneal agents especially when planning possible phase III trials.
The morbidity and mortality of this local-regional therapeutic modality is high but likely to improve as experience is accumulated. The incidence of total morbidity reported in some studies [17, 18] was 45%–60%. The incidence of anastomotic leaks and bowel fistulas ranged from 0% to 12%; this may be acceptable considering that many of the patients have been heavily pretreated with chemotherapy. Similarly, the mortality was <10% but it should be emphasized that two of the centers with the largest experience reported series with no perioperative deaths [10, 12]. As with other complex procedures, it appears that a learning curve exists that correlates with outcomes [20]. Most of the serious morbidity arose from the surgical aspect of the procedure while drug-related toxicity from intraperitoneal chemotherapy was usually mild. This again illustrates that patient selection is of paramount importance for this procedure to be used successfully. Considering that the incidence of serious complications is <20% in most series and the median mortality 3% (range 0%–10%), it seems reasonable to attempt to integrate this combined treatment into the management of ovarian cancer.
We limited this systematic review to studies that met strict inclusion criteria. This eliminated publications reporting the experience using this abdominopelvic treatment in ovarian cancer combined with other causes of carcinomatosis as well as studies using heated intraoperative intraperitoneal chemotherapy without major cytoreduction [34–40] or with repeated postoperative treatments [5]. The results of these publications provide additional support for the use of heated intraoperative intraperitoneal chemotherapy in ovarian cancer.
The survivals reported with cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy may be superior to the results of conventional treatment. With systemic chemotherapy, patients with platinum-sensitive recurrent disease have an overall median survival of 29 months [41] while patients with platinum-resistant disease have an overall survival of only 17 months [42]. In contrast, overall survival of 22–45 months in patients treated with cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy is promising considering that most of the studies included a large number of patients with recurrent disease. The retrospective nature and the extreme heterogeneity of the studies limit our ability to make conclusive statements about the benefit of this method. Also, no cost-benefit analyses regarding this new approach are available. Patient selection bias has likely influenced the outcomes. These results indicate that selected patients with recurrent ovarian cancer could be considered candidates for salvage therapy with cytoreductive surgery and heated perioperative intraperitoneal chemotherapy and the efficacy of this combined treatment should be evaluated in a prospective phase III trial. In the subgroup of patients with platinum-resistant recurrent ovarian cancer, alternative drugs like mitomycin C, melphalan or docetaxel (Taxotere®; Aventis Pharma, Antony, Cedex, France) should replace platinum in the intraperitoneal chemotherapy regimen [43].
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This study was supported by the Foundation for Applied Research in Gastrointestinal Oncology.
Received for publication January 8, 2007. Revision received March 15, 2007. Accepted for publication March 22, 2007.
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