HIPEC for gynaecological malignancies: A last update (Review)
- Authors:
- Published online on: May 4, 2023 https://doi.org/10.3892/mi.2023.85
- Article Number: 25
-
Copyright: © Margioula-Siarkou et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
1. Introduction
The possibility of developing peritoneal metastases (PM) is increased in patients with malignancies of the digestive system or gynaecological cancer. The treatment of PM has changed significantly over the past years; therefore, colorectal malignancies, appendicular malignancies, mesotheliomas and primary ovarian cancer are currently being managed with improved survival outcomes (1). Hyperthermic intraperitoneal chemotherapy (HIPEC) following cytoreductive surgery (CRS) has been a method gaining increasing interest in the context of the treatment of peritoneal malignancy over the past years. HIPEC involves the administration of anticancer drugs directly into the abdominal cavity for peritoneal lesions, as well as intraperitoneal administration, accompanied by heated chemotherapeutic agents that are administered immediately after cytoreduction. Based on some of the previously published evidence, HIPEC plus CRS is considered to offer a prognostic advantage for patients with primary peritoneal tumors or PM from colorectal, gastric and ovarian cancer (2-6). Nonetheless, HIPEC plus CRS has not yet been established as a standard of care. Furthermore, in particular, as regards gynaecological malignancies, it remains a question whether HIPEC may be one of the novel therapeutic strategies for other gynaecological malignancies, such as endometrial and cervical cancer with peritoneal expansion, as well as peritoneal sarcomatosis. The lack of prospective studies and small sample sizes of already published articles have made it rather difficult to reach a definite consensus.
The present review summarizes the current evidence on the therapeutic role of HIPEC in various gynaecological malignancies, indicate those cancer types and settings in which HIPEC has an evidence-based beneficial impact. Furthermore, the present review highlights potential safety issues and concerns associated with the use of HIPEC, issues which remain to be answered by researchers.
2. Data collection methods
The present review presents a summary of the current literature, summarizing evidence retrieved from evidence dealing with the clinical impact of HIPEC regarding treatment of gynaecological malignancies, namely primary and recurrent ovarian cancer, endometrial cancer, cervical cancer and peritoneal sarcomatosis. A manual search was conducted using the PubMed and Scopus databases with the key phrases/key words, ‘HIPEC AND ovarian cancer’, ‘HIPEC AND endometrial cancer’, ‘HIPEC AND cervical cancer’, ‘HIPEC AND peritoneal sarcomatosis’. Prospective randomized clinical trials (RCTs), prospective observational studies and meta-analyses written in the English language were set in the centre of interest for interpretation of their results. Retrospective studies, in the absence of higher-level evidence, were also considered for the purpose of the present review. Main survival outcomes set in the centre of interest were disease-free survival (DFS), overall survival (OS), overall recurrence and mortality. Furthermore, evidence of the safety of the methods was studied, specifically in the rate of complications, mainly 3 and 4, according to the Clavien-Dildo (CD) classification, as well as overall morbidity through the emergence of post-operative complications (POCs), in an effort to examine whether HIPEC significantly increases their incidence and thereafter evaluate their impact on overall survival parameters.
3. Primary ovarian cancer
Over the years, various trials have been conducted in an attempt to clarify the role of HIPEC in addition to CRS for the treatment of advanced ovarian cancer as regards both the primary and neoadjuvant setting. According to the current literature, HIPEC can be used at the time of first-line therapy, i.e., at the time of primary CRS (upfront CRS and HIPEC), or at the time of interval CRS, which is performed following neoadjuvant chemotherapy (interval CRS and HIPEC), but cannot be considered as a standard of care. Moreover, HIPEC can be used along with CRS performed as second-line therapy, in patients who have had suboptimal surgery followed by chemotherapy and therefore, have residual disease (secondary CRS and HIPEC), or in patients who have recurred after complete response to first line therapy (salvage CRS and HIPEC) (7,8). Deraco et al (9) were the first to provide evidence suggesting that HIPEC following CRS may have auspicious results (that are at least comparable) for primary advance-stage ovarian cancer in terms of OS and progression-free survival (PFS) when compared to control populations of previously published trials (10-13). Lim et al (14), monitoring 184 women with stage III or IV primary advanced ovarian cancer that underwent primary or interval cytoreductive surgery with or without the addition of HIPEC, indicated no significant improvement in the rate of PFS or OS between the two groups as regards the overall population of patients. However, when performing a sub-analysis separately for primary cytoreduction surgery and for interval debulking surgery, they indicated that in the neoadjuvant-treatment group, HIPEC + CRS led to a significant improvement in PFS compared with only CRS (14). Consistent with these data were the findings of van Driel et al (15) and Antonio et al (16), demonstrating that the addition of HIPEC to the interval CRS in patients with advanced ovarian cancer treated with neoadjuvant chemotherapy significantly improved DFS (by 3.5 and 6 months, respectively) and OS (by 11.8 and 7 months, respectively). Thereafter, even if the results for primary surgery are rather conflicting to support supremacy of HIPEC, there are still three RCTs firmly supporting the beneficial effects of HIPEC for patients with advanced-stage ovarian cancer (14-16).
As regards the safety of the method, HIPEC + CRS have been shown to be associated with a similar rate of grade 3 or 4 adverse events, along with lower disease recurrence or mortality rate compared to the surgery-only group, without negatively affecting the quality of life of patients and the incidence of POCs, while it was not identified as economically disadvantageous (17,18). Nonetheless, given the need for further research in this field, current clinical trials focus on assessing the potential superiority of this novel approach for epithelial ovarian carcinoma (EOC) in terms of efficacy, safety, treatment feasibility and quality of life (19).
It is evident that further research needs to be performed in this field. In this context, the study by Koole et al (20) attempted to determine the role of HIPEC by assigning 538 patients with FIGO stage III EOC to CRS with or without HIPEC. Likewise, the prospective multi-centre randomized trial, CHIPPI 1808(19), which randomized 432 patients with stage III EOC, aimed to assess the potential superiority of the addition of HIPEC on the efficacy, safety, treatment feasibility, and patient quality of life.
However, based on the findings of already published trials, HIPEC plus CRS appears to have a beneficial effect on the survival outcomes of patients with advanced-stage ovarian cancer following neoadjuvant chemotherapy; however, the question remains regarding whether it is beneficial following primary cytoreduction surgery. Table I represents the main outcomes of studies dealing with the role of HIPEC in the treatment of primary ovarian cancer. A point worth mentioning, is that apart from the study by Deraco et al (9), which was a prospective study analysing the treatment of only one group of patients, the other three studies are similarly designed (14-16). They are prospective randomized trials comparing arms, where cisplatin is used and mainly NACH is followed by either CRS plus HIPEC or CRS alone.
 | Table IMain studies and the comparative outcomes of studies comparing the effects of HIPEC in the treatment of EOC. |
4. Recurrent ovarian cancer
Recurrent ovarian cancer often represents a challenging clinical entity, where various treatment modalities need to be individualized in an effort to optimize patient survival outcomes. HIPEC has also been proposed as an alternative modality of treatment combined with secondary CRS and followed by systematic chemotherapy. Spiliotis et al (21) presented the first phase 3 randomized controlled trial of 120 patients. The results indicated that both the mean OS (26.7 vs. 13.4 months, P=0.006) and 3-year OS (75 vs. 18%, P<0.01) were significantly improved following CRS and HIPEC vs. surgery alone. That study also highlighted that optimal cytoreduction appears to be an independent prognostic factor for OS. Furthermore, in the HIPEC group, a similar mean OS was achieved for both platinum-sensitive and platinum-resistant disease, which may lead to the conclusion that the addition of HIPEC rather eliminated the detrimental effect of platinum resistance (21). By contrast, a more recent randomized phase II trial by Zivanovic et al (22) did not demonstrate any comparative advantage of HIPEC plus CRS vs. CRS only as regards OS and DFS. Based on a ‘pick-the-winner’ design, an arm would be considered superior if at least 17 out of 49 patients were without progression at 24 months follow-up, which was accomplished in none of the arms.
Thereafter, as there are two prospective studies (21,22) with conflicting outcomes, no definitive conclusions may be deduced on the effects of HIPEC on recurrent ovarian cancer. The outcomes of aforementioned ongoing trials may also contribute to reaching conclusions in the field of research in recurrent ovarian cancer as well. HIPEC remains an experimental therapy with potential harm, and should only be offered in the context of well-designed, prospective RCTs, since the feasibility and the efficacy as a second-line treatment have yet to be established. Table II presents the main outcomes of studies comparing the effects of HIPEC in the treatment of recurrent EOC, as they arise from two prospective randomized studies, where different chemotherapeutic agent regimens are used and disparate arms in between are compared, since in one study in the treatment of all patients was included the systematic CH.
| Table IIMain studies and the comparative outcomes of studies comparing the effects of HIPEC in the treatment of recurrent EOC. |
5. Endometrial cancer
Endometrial cancer is the most common female pelvic malignancies, with an incidence rate of 4% (23). Nonetheless, the survival outcomes of patients with endometrial cancer and PM warrant improvement. Tempfer et al (24), in a recent systematic review, identified 68 women from eight articles with EC-derived PM that underwent CRS and HIPEC as a therapeutic strategy, the majority of which (46/patients) also received post-operative systemic chemotherapy. At the time of the surgery, the peritoneal carcinomatosis index (PCI) was 16.7 and a macroscopically complete cytoreduction (CC)-0 was achieved in 44/63 (70%) of the patients. The analysis concluded that the median DFS and OS times ranged from 7 to 18 months and from 12 to 33 months, respectively. Of note, the percentage of treatment-associated mortality was 1% (1/63), while adverse events of grade 3 and 4 were observed in 18/63 (28%) patients (24). Despite the fact that these data are not comparative, they rather indicate that HIPEC may be a safe and effective option for advanced-stage endometrial cancer with PM; however, no evidence from prospective studies comparing CRS + HIPEC vs. only CRS is yet available to support beneficial impact of HIPEC in such patients.
Of note, another more recent multi-institutional study performed on 60 patients with peritoneal progression of EC reported no significant advantage from the combination of HIPEC plus CRS on the examined parameters of DFS and OS compared with CRS monotherapy (25). Nonetheless, that study was limited by its retrospective nature and by the fact that in the ‘CRS plus HIPEC’ group, 96.7% of women were treated for recurrence, whereas in the ‘CRS only’ group, 83.3% were treated for primary disease.
In conclusion, the combination of CRS and HIPEC for advanced-stage EC with PM has been proposed as having promising outcomes, constituting a safe and feasible approach with an acceptable morbidity and mortality rate. However, to date, there is no evidence supporting a beneficial effect of HIPEC addition to standard treatment; therefore, prospective comparative clinical trials are warranted to further explore this potential. Table III represents the main outcomes of studies dealing with the efficacy of HIPEC in the treatment of advanced-stage EC. The disparities between the two studies, need to be taken into consideration, with the one being a systematic review reporting only patients undergoing CRS plus HIPEC and in some cases accompanied by systematic chemotherapy, and the other being a retrospective non-randomized study comparing two different treatment strategies (24,25).
| Table IIIMain studies and the comparative outcomes of studies comparing the effects of HIPEC in the treatment of endometrial cancer. |
6. Peritoneal sarcomatosis
While the role of CRS plus HIPEC in peritoneal carcinomatosis has been well-documented, its utility in peritoneal sarcomatosis remains unproven. The applications of CRS and HIPEC were analysed by a recent meta-analysis by Wong et al (26), in which 16 studies with 320 women were included. The mean PCI was 11.8 and 79.3% out of 256 subjects who achieved CC-0 cytoreduction. Furthermore, that study reported that these techniques managed to significantly increase the median OS, compared to the conventional treatments, in which the prognosis is still reported to be poor (median survival ranging from 13 to 18 months) (27,28). According to that study (26), the overall pooled median OS was 29.3 months (95% CI, 23.8-34.8), with a 5-year OS of 35.3% (95% CI, 26.3-44.8), the median DFS was 12.0 months (95% CI, 8.0-16.0) and the 5-year DFS was 21.8% (95% CI, 13.2-31.7). Of note, the subgroup analysis resulted in a pooled median OS of 33.5 months for leiomyosarcomas and 39.1 months for liposarcomas, indicating the discrepant response between the various histological subtypes. In addition, patients with CC-0 cytoreduction had a higher median OS of 34.6 months (95% CI: 23.2-45.9), suggesting once more that the maximal cytoreduction is a favourable prognostic marker. The percentage of severe complications (grade ≥3) was 17.4% (95% CI: 9.8-26.3).
In summary, HIPEC appears to be an effective therapeutic alternative for selected patients with PS and a low tumour burden. However, a safe conclusion cannot be drawn, since the majority of the studies were retrospective single arm studies, while the rarity of the disease often led to compromised the sample size. Therefore, further studies involving a direct comparison between HIPEC, CRS and conventional treatments are required to comprehensively assess the effects of this method.
7. Cervical cancer
Cases of cervical cancer involving the recurrence of peritoneal carcinomatosis remain limited. Recently, the effects of HIPEC plus CRS f or such patients were analysed by Duzgun and Kalin (29). They performed a retrospective analysis including 10 cases of women who underwent HIPEC plus CRS following the occurrence of intraabdominal metastases. The mean average of the PCI score was 12.3 (range, 7-36) and the mean average of completeness of cytoreduction score was 1 in 2 patients and 0 in 8 patients. During the first 30 days post-operatively no mortality was recorded, while grade 3 complications were reported in 5 cases (50%). In the early period of 3 years post-operatively, 4 patients succumbed at 2, 5, 6 and 12 months, respectively. Based on the findings of that study, no definite consensus can be made on whether there is any sign of benefit in advanced-stage cervical cancer with PM, both due to high complication rate and the short-expected OS in the early period in patients at this stage of the disease. Furthermore, Lantsman et al (30) published their results on 2 cases of recurrent cervical cancer with peritoneal carcinomatosis, in which HIPEC was implemented during debulking surgery. Notably, patients displayed a substantial DFS time of 15 and 24 months, respectively. In conclusion, there is no sufficient evidence regarding HIPEC implementation in cervical cancer patients with peritoneal recurrence. The published literature is rather limited and may offer inadequate evidence in terms of efficacy and safety. The only relevant evidence includes publications, both presenting retrospectively the implementation of HIPEC plus CRS in a very limited number of patients. However, HIPEC may be considered as an alternative for symptomatic patients with peritoneal recurrence when alternative treatment options are considered of poor effectiveness on an individualized basis.
8. HIPEC complications
A special concern about HIPEC implementation is considered to be the safety and risk for intraoperative and mostly POCs. Although the majority of the complications according to the CD classification may be attributed to CRS itself, the possibility that HIPEC increases the morbidity cannot be ruled out. In the study by van Driel et al (15), it was reported that in each group, >95% of the patients had a minimum of one adverse event of any grade until the last cycle of chemotherapy, although no significant difference was observed between the two groups. Additionally, as regards the incidence of grade 3 or 4 adverse events, both the control and intervention group presented comparable numbers (25% in the surgery group and 27% in the surgery-plus-HIPEC group, P=0.76). Although the most common adverse events were abdominal pain, infection and ileus, an increased rate of infection, thromboembolic, pulmonary and electrolyte disturbance events were noted particularly in the HIPEC group. As for the rates of completion of all three cycles of chemotherapy after surgery and the median total length of hospital admission, both values were also similar between the groups (15). In summary, according to recent literature, the addition of HIPEC is not associated with significantly higher rates of complications (24,25).
Interesting observations of POCs with HIPEC may be derived from the results published by US HIPEC Collaborative, even though this did not concern gynaecological malignancies, but HIPEC for appendiceal/colorectal disease (31). Gamboa et al (31) reported POCs of patients who underwent CCR0/1 surgery with CRS and HIPEC for appendiceal/colorectal cancer. As their analysis was stratified by non-invasive vs. invasive disease, they highlighted that complications were associated with a decreased OS and RFS for invasive histology, which was not the case for non-invasive neoplasms. Specifically, their study manifested that the presence of any POC was connected with a decreased 3-year OS (59 vs. 74%; P<0.001) and RFS (32 vs. 42%; P<0.001) for invasive appendiceal neoplasms. Of all types of adverse events, a substantially higher proportion was regarded as infectious complications in both types, which can further induce inflammatory responses that prolong the aforementioned pro-metastatic processes.
In conclusion, the combination of HIPEC plus CRS, when compared to traditional methods, does not have a significant effect on the incidence of POCs, type of grade 3 or 4 adverse events, safety and health-related quality-of-life outcomes. However, since POCs are associated with a decreased OS and RFS in certain groups of patients, further research is required targeting the optimal practices and standardized prevention strategies, alongside with proper patient selection.
9. Conclusions and future perspectives
Over the past few years, the use of HIPEC following CRS for the treatment of peritoneal malignancies has exhibited an increasing trend. HIPEC entails the intraperitoneal delivery of heated chemotherapeutic agents straight into the abdominal cavity for peritoneal lesions following cytoreduction. The heating of the abdominal cavity, in particular by maintaining the temperature at 41 to 43˚C, can itself have a direct antitumor effect, and it can enhance the antitumor effect and tissue migration of certain anticancer agents, such as cisplatin, mitomycin C and oxaliplatin. The team can choose to administer treatment for 60 to 90 min, either by open or close method one or a combination of the following agents: Cisplatin (40-100 mg/m2), doxorubicin (35 mg/m2), paclitaxel (175 mg/m2), carboplatin (800 mg/m2) or mitomycin (15 mg/m2). To the best of our knowledge, HIPEC has been studied mainly as a first-line treatment for gynaecological malignancies and only for recurrent ovarian cancer as a second line-treatment in a wider range. This novel method has not been proven to be beneficial in appropriately designed prospective studies, with only a few case reports or case series reporting encouraging results regarding its role as a consolidation therapy, following the completion of first-line therapy of ovarian cancer, along with second-look surgery (consolidation CRS and HIPEC) or as a second-line treatment of gynaecological cancer and peritoneal carcinomatosis from gynaecological malignancies (8,30,32,33). In summary, there is sufficient evidence from three prospective RCTs that HIPEC has a beneficial effect in patients with advanced-stage ovarian cancer after neoadjuvant chemotherapy (14-16). Specifically, when compared with CRS alone, HIPEC provides an advantage in terms of OS and DFS, while rates of adverse events are comparable. There is also level-I evidence supporting the beneficial effect of HIPEC also for recurrence of ovarian cancer. However, as it is only one RCT supporting therapeutic supremacy and results are disputed by those of another prospective phase II trial, no definitive conclusion may be made and still research need to be performed. Existing evidence does not support the benefit of HIPEC addition to primary surgery for EOC. Furthermore, as regards peritoneal sarcomatosis, endometrial and cervical cancer, studies are not sufficient to support the benefit of this approach, even if results still appear promising. The addition of HIPEC is not significantly associated with higher rates of POCs. Cisplatin appears to be the chemotherapeutic agent of choice. Finally, of note, as is indicated by the publications on HIPEC, CC with no residual disease remains the main and mostly determining prognostic factor, particularly for patients with ovarian cancer. Thus, the key message may be that the addition of HIPEC to CRS may not be considered as a substitute of non-optimal surgery, but as a beneficial addition to optimize results following CC. Moreover, of paramount importance is the evaluation of a multidisciplinary approach regarding these types of malignancies. Over the course of the years, several studies have attempted to indicate the beneficial role of the multidisciplinary tumour boards (MTBs) (34). In a recent systematic literature review regarding multidisciplinary approach in cancer patients, the adherence to clinical guidelines and the improvement in patient outcomes was indicated, although it was often associated with an increase in expenditure costs and not always with a significant impact on the prognosis of patients (35). There are studies which have highlighted that the patient-cantered care approach improved the management and decision-making process, particularly in multifactorial malignancy types, such as ovarian cancer (36,37). When allocating the optimal treatment, the crucial factor becomes the selection criteria for each strategy, and to determine which group would be benefit from each treatment by individualizing the approach. In order for this to be accomplished, the multimodal tumour board consists of experts, who evaluate patients' characteristics and tumour behaviour. Defining the clinical criteria for different strategies and applying a structured algorithm may help maximize the overall outcome and minimize the overall treatment-related morbidity and mortality, particularly when patients are treated in specialized structures where multidisciplinary teams operate (36,37). Moreover, in the concept of personalized treatment, the most effect strategy to minimize heterogeneity is by an expert consensus that aims to identify and define a limited number of regimens for each indication and primary site. At this point, selections of the regimen can then be tailored to the patient profile and its expected toxicity and the methodology according regional factors (38). The analysis of the BRCA mutational status has allowed the first step into individualized strategies for the management of patients with ovarian cancer. A large number of BRCA1/2 mutations have been described over the years, and several of these are reliably known to increase cancer susceptibility (39). BRCA mutations confer various properties, including increased response to DNA-damaging agents such as platinum-based chemotherapy and poly-ADP-ribose polymerase (PARP) inhibitor. The treatment armamentarium has recently been expanded by the addition of targeted therapies, including bevacizumab, a humanized monoclonal antibody against vascular endothelial growth factor (VEGF) and PARP inhibitors. These have recently been approved for the treatment of ovarian cancer, based on the findings of RCTs that demonstrated significant benefits in terms of progression-free survival, with acceptable tolerability and no negative effects on the quality of life. Olaparib, the first PARP inhibitor approved, is currently used as maintenance monotherapy in patients with ovarian cancer who have relapsed disease and a mutated BRCA gene, and have achieved a complete or partial response to platinum-based chemotherapy. As a result, determining the BRCA mutation status has become critical for therapeutic decisions (40,41). It would of interest if the efficacy of HIPEC could also be demonstrated in a large scale of selective patient groups stratified by the BRCA1/2 positive status. Although it is not extensively studied, there is some retrospective evidence that suggests a possible increase in efficacy in this population (42,43). As regards the addition of the anti-VEGF monoclonal antibody, bevacizumab, to the carboplatin-paclitaxel regimen, as reported in the ICON7 and GOG-0218 phase 3 studies, it remains the only treatment that has prolonged PFS (44,45). An innovative technique that is used to treat primary peritoneal malignancies, as well as carcinomatosis originating from various tumours is bidirectional intraoperative chemotherapy. It involves the intraoperative simultaneous administration of intravenous chemotherapy and HIPEC, immediately after CRS. This technique in combination with bevacizumab has been studied by Walker et al (46), comparing intravenous vs. intraperitoneal chemotherapy plus bevacizumab in advanced ovarian carcinoma; however, no statistically significant increase was reported in the duration of PFS with either regimen. Large multicentre well-designed RCTs are still required to explore all the spectrum of potential therapeutic usage of HIPEC to treat advanced-stage gynaecological cancer.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
Not applicable.
Authors' contributions
CMS was a major contributor to the writing of the manuscript. CMS, AA, KD and SP were responsible for the collection of the relevant literature for inclusion in the review. AP, ASL, GM and FG revised the manuscript critically for important intellectual content. All authors have read and approved the final manuscript. Data authentication is not applicable.
Ethics approval and consent to participate
Not applicable.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
|
Rajan F and Bhatt A: Management of peritoneal metastases-cytoreductive surgery, HIPEC and beyond. Springer. 2018. | |
|
Yan TD, Welch L, Black D and Sugarbaker PH: A systematic review on the efficacy of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for diffuse malignancy peritoneal mesothelioma. Ann Oncol. 18:827–834. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Goéré D, Passot G, Gelli M, Levine EA, Bartlett DL, Sugarbaker PH and Glehen O: Complete cytoreductive surgery plus HIPEC for peritoneal metastases from unusual cancer sites of origin: Results from a worldwide analysis issue of the peritoneal surface oncology group international (PSOGI). Int J Hyperthermia. 33:520–527. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Hotouras A, Desai D, Bhan C, Murphy J, Lampe B and Sugarbaker PH: Heated IntraPEritoneal chemotherapy (HIPEC) for patients with recurrent ovarian cancer: A systematic literature review. Int J Gynecol Cancer. 26:661–670. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Kireeva GS, Gafton GI, Guseynov KD, Senchik KY, Belyaeva OA, Bespalov VG, Panchenko AV, Maydin MA and Belyaev AM: HIPEC in patients with primary advanced ovarian cancer: Is there a role? A systematic review of short- and long-term outcomes. Surg Oncol. 27:251–258. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Honoré C, Goéré D, Macovei R, Colace L, Benhaim L and Elias D: Peritoneal carcinomatosis from unusual cancer origins: Is there a role for hyperthermic intraperitoneal chemotherapy? J Visc Surg. 153:101–107. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Mulier S, Claes JP, Dierieck V, Amiel JO, Pahaut JP, Marcelis L, Bastin F, Vanderbeeken D, Finet C, Cran S and Velu T: Survival benefit of adding hyperthermic IntraPEritoneal chemotherapy (HIPEC) at the different time-points of treatment of ovarian cancer: Review of evidence. Curr Pharm Des. 18:3793–3803. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Bae JH, Lee JM, Ryu KS, Lee YS, Park YG, Hur SY, Ahn WS and Namkoong SE: Treatment of ovarian cancer with paclitaxel- or carboplatin-based intraperitoneal hyperthermic chemotherapy during secondary surgery. Gynecol Oncol. 106:193–200. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Deraco M, Kusamura S, Virzì S, Puccio F, Macrì A, Famulari C, Solazzo M, Bonomi S, Iusco DR and Baratti D: Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy as upfront therapy for advanced epithelial ovarian cancer: Multi-institutional phase-II trial. Gynecol Oncol. 122:215–220. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Vergote I, Tropé CG, Amant F, Kristensen GB, Ehlen T, Johnson N, Verheijen RH, van der Burg ME, Lacave AJ, Panici PB, et al: Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N Engl J Med. 363:943–953. 2010.PubMed/NCBI View Article : Google Scholar | |
|
Chi DS, Eisenhauer EL, Zivanovic O, Sonoda Y, Abu-Rustum NR, Levine DA, Guile MW, Bristow RE, Aghajanian C and Barakat RR: Improved progression-free and overall survival in advanced ovarian cancer as a result of a change in surgical paradigm. Gynecol Oncol. 114:26–31. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Armstrong DK, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, Copeland LJ, Walker JL and Burger RA: Gynecologic Oncology Group. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med. 354:34–43. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Eisenkop SM, Spirtos NM, Friedman RL, Lin WC, Pisani AL and Perticucci S: Relative influences of tumor volume before surgery and the cytoreductive outcome on survival for patients with advanced ovarian cancer: A prospective study. Gynecol Oncol. 90:390–396. 2003.PubMed/NCBI View Article : Google Scholar | |
|
Lim MC, Chang SJ, Park B, Yoo HJ, Yoo CW, Nam BH and Park SY: HIPEC for Ovarian Cancer Collaborators. Survival after hyperthermic intraperitoneal chemotherapy and primary or interval cytoreductive surgery in ovarian cancer: A randomized clinical trial. JAMA Surg. 157:374–383. 2022.PubMed/NCBI View Article : Google Scholar | |
|
van Driel WJ, Koole SN, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RHM, de Hingh IHJT, van der Velden J, Arts HJ, Massuger LFAG, et al: Hyperthermic intraperitoneal chemotherapy in ovarian cancer. N Engl J Med. 378:230–240. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Antonio CCP, Alida GG, Elena GG, Rocío GS, Jerónimo MG, Luis ARJ, Aníbal ND, Francisco BV, Jesús GRÁ, Pablo RR and José GM: Cytoreductive surgery with or without HIPEC after neoadjuvant chemotherapy in ovarian cancer: A Phase 3 clinical trial. Ann Surg Oncol. 29:2617–2625. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Koole SN, Kieffer JM, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RH, de Hingh IH, van der Velden J, Arts HJ, van Ham MAPC, et al: Health-related quality of life after interval cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy (HIPEC) in patients with stage III ovarian cancer. Eur J Surg Oncol. 47:101–107. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Koole SN, van Lieshout C, van Driel WJ, van Schagen E, Sikorska K, Kieffer JM, Schagen van Leeuwen JH, Schreuder HWR, Hermans RH, de Hingh ICH, et al: Cost effectiveness of interval cytoreductive surgery with hyperthermic intraperitoneal chemotherapy in stage III ovarian cancer on the basis of a randomized phase III trial. J Clin Oncol. 37:2041–2050. 2019.PubMed/NCBI View Article : Google Scholar | |
|
El Hajj H, Vanseymortier M, Hudry D, Bogart E, Abdeddaim C, Leblanc E, Le Deley MC and Narducci F: Rationale and study design of the CHIPPI-1808 trial: A phase III randomized clinical trial evaluating hyperthermic intraperitoneal chemotherapy (HIPEC) for stage III ovarian cancer patients treated with primary or interval cytoreductive surgery. ESMO Open. 6(100098)2021.PubMed/NCBI View Article : Google Scholar | |
|
Koole S, van Stein R, Sikorska K, Barton D, Perrin L, Brennan D, Zivanovic O, Mosgaard BJ, Fagotti A, Colombo PE, et al: Primary cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy (HIPEC) for FIGO stage III epithelial ovarian cancer: OVHIPEC-2, a phase III randomized clinical trial. Int J Gynecol Cancer. 30:888–892. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Spiliotis J, Halkia E, Lianos E, Kalantzi N, Grivas A, Efstathiou E and Giassas S: Cytoreductive surgery and HIPEC in recurrent epithelial ovarian cancer: A prospective randomized phase III study. Ann Surg Oncol. 22:1570–1575. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Zivanovic O, Chi DS, Zhou Q, Iasonos A, Konner JA, Makker V, Grisham RN, Brown AK, Nerenstone S, Diaz JP, et al: Secondary cytoreduction and carboplatin hyperthermic intraperitoneal chemotherapy for platinum-sensitive recurrent ovarian cancer: An MSK team ovary phase II study. J Clin Oncol. 39:2594–2604. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Jamison PM, Altekruse SF, Chang JT, Zahn J, Lee R, Noone AM and Barroilhet L: Site-specific factors for cancer of the corpus uteri from SEER registries: Collaborative stage data collection system, version 1 and version 2. Cancer. 120:3836–3845. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Tempfer CB, Kern P, Dogan A, Hilal Z and Rezniczek GA: Cytoreductive surgery with hyperthermic intraperitoneal chemotherapy for endometrial cancer-derived peritoneal metastases: A systematic review. Clin Exp Metastasis. 36:321–329. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Gomes David M, Bakrin N, Salleron J, Kaminsky MC, Bereder JM, Tuech JJ, Lehmann K, Mehta S, Glehen O and Marchal F: Cytoreductive surgery (CRS) plus hyperthermic intraperitoneal chemotherapy (HIPEC) vs CRS alone for treatment of endometrial cancer with peritoneal metastases: A multi-institutional study from PSOGI and BIG RENAPE groups. BMC Surg. 22(1)2022.PubMed/NCBI View Article : Google Scholar | |
|
Wong LCK, Li Z, Fan Q, Tan JW, Tan QX, Wong JSM, Ong CJ and Chia CS: Cytoreductive surgery (CRS) with hyperthermic intraperitoneal chemotherapy (HIPEC) in peritoneal sarcomatosis-A systematic review and meta-analysis. Eur J Surg Oncol. 48:640–648. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Anaya DA, Lahat G, Liu J, Xing Y, Cormier JN, Pisters PW, Lev DC and Pollock RE: Multifocality in retroperitoneal sarcoma: A prognostic factor critical to surgical decision-making. Ann Surg. 249:137–142. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Bilimoria MM, Holtz DJ, Mirza NQ, Feig BW, Pisters PW, Patel S, Pollock RE, Benjamin RS, Papadopoulos NE, Plager C, et al: Tumor volume as a prognostic factor for sarcomatosis. Cancer. 94:2441–2446. 2002.PubMed/NCBI View Article : Google Scholar | |
|
Duzgun O and Kalin M: Is cytoreductive surgery possible in cervical cancer peritoneal carcinomatosis? Clin Med Insights Oncol. 15(11795549211065308)2021.PubMed/NCBI View Article : Google Scholar | |
|
Lantsman T, Lepe M, Garrett L, Goodman M and Shea M: Management of recurrent cervical cancer with peritoneal carcinomatosis with HIPEC. Gynecol Oncol Rep. 39(100909)2021.PubMed/NCBI View Article : Google Scholar | |
|
Gamboa AC, Lee RM, Turgeon MK, Zaidi MY, Kimbrough CW, Grotz TE, Leiting J, Fournier K, Lee AJ, Dineen SP, et al: Implications of postoperative complications for survival after cytoreductive surgery and HIPEC: A multi-institutional analysis of the US HIPEC collaborative. Ann Surg Oncol. 27:4980–4995. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Sugarbaker PH: Survival of large volume recurrent endometrial cancer with peritoneal metastases treated by cytoreductive surgery, HIPEC and EPIC. Report of a case. Int J Surg Case Rep. 80(105669)2021.PubMed/NCBI View Article : Google Scholar | |
|
de Bree E, Romanos J, Michalakis J, Relakis K, Georgoulias V, Melissas J and Tsiftsis DD: Intraoperative hyperthermic intraperitoneal chemotherapy with docetaxel as second-line treatment for peritoneal carcinomatosis of gynaecological origin. Anticancer Res. 23:3019–3027. 2003.PubMed/NCBI | |
|
Croke JM and El-Sayed S: Multidisciplinary management of cancer patients: Chasing a shadow or real value? An overview of the literature. Curr Oncol. 19:e232–e238. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Berardi R, Morgese F, Rinaldi S, Torniai M, Mentrasti G, Scortichini L and Giampieri R: Benefits and limitations of a multidisciplinary approach in cancer patient management. Cancer Manag Res. 12:9363–9374. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Falzone L, Scandurra G, Lombardo V, Gattuso G, Lavoro A, Distefano AB, Scibilia G and Scollo P: A multidisciplinary approach remains the best strategy to improve and strengthen the management of ovarian cancer (review). Int J Oncol. 59(53)2021.PubMed/NCBI View Article : Google Scholar | |
|
Aletti GD, Garbi A, Messori P, Achilarre MT, Zanagnolo V, Rizzo S, Alessi S, Bocciolone L, Landoni F, Biffi , et al: Multidisciplinary approach in the management of advanced ovarian cancer patients: A personalized approach. Results from a specialized ovarian cancer unit. Gynecol Oncol. 144:468–473. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Bhatt A, de Hingh I, Van Der Speeten K, Hubner M, Deraco M, Bakrin N, Villeneuve L, Kusamura S and Glehen O: HIPEC methodology and regimens: The need for an expert consensus. Ann Surg Oncol. 28:9098–9113. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Cline MS, Liao RG, Parsons MT, Paten B, Alquaddoomi F, Antoniou A, Baxter S, Brody L, Cook-Deegan R, Coffin A, et al: BRCA challenge: BRCA exchange as a global resource for variants in BRCA1 and BRCA2. PLoS Genet. 14(e1007752)2018.PubMed/NCBI View Article : Google Scholar | |
|
Gadducci A, Guarneri V, Peccatori FA, Ronzino G, Scandurra G, Zamagni C, Zola P and Salutari V: Current strategies for the targeted treatment of high-grade serous epithelial ovarian cancer and relevance of BRCA mutational status. J Ovarian Res. 12(9)2019.PubMed/NCBI View Article : Google Scholar | |
|
Lavoro A, Scalisi A, Candido S, Zanghì GN, Rizzo R, Gattuso G, Caruso G, Libra M and Falzone L: Identification of the most common BRCA alterations through analysis of germline mutation databases: Is droplet digital PCR an additional strategy for the assessment of such alterations in breast and ovarian cancer families? Int J Oncol. 60(58)2022.PubMed/NCBI View Article : Google Scholar | |
|
Madariaga A, Lheureux S and Oza AM: Tailoring ovarian cancer treatment: implications of BRCA1/2 mutations. Cancers (Basel). 11(416)2019.PubMed/NCBI View Article : Google Scholar | |
|
Safra T, Grisaru D, Inbar M, Abu-Abeid S, Dayan D, Matceyevsky D, Weizman A and Klausner JM: Cytoreduction surgery with hyperthermic intraperitoneal chemotherapy in recurrent ovarian cancer improves progression-free survival, especially in BRCA-positive patients-a case-control study. J Surg Oncol. 110:661–665. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Oza AM, Cook AD, Pfisterer J, Embleton A, Ledermann JA, Pujade-Lauraine E, Kristensen G, Carey MS, Beale P, Cervantes A, et al: Standard chemotherapy with or without bevacizumab for women with newly diagnosed ovarian cancer (ICON7): Overall survival results of a phase 3 randomised trial. Lancet Oncol. 16:928–936. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Monk BJ, Huang HQ, Burger RA, Mannel RS, Homesley HD, Fowler J, Greer BE, Boente M, Liang SX and Wenzel L: Patient reported outcomes of a randomized, placebo-controlled trial of bevacizumab in the front-line treatment of ovarian cancer: A gynecologic oncology group study. Gynecol Oncol. 128:573–578. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Walker JL, Brady MF, Wenzel L, Fleming GF, Huang HQ, DiSilvestro PA, Fujiwara K, Alberts DS, Zheng W, Tewari KS, et al: Randomized trial of intravenous versus intraperitoneal chemotherapy plus bevacizumab in advanced ovarian carcinoma: An NRG oncology/gynecologic oncology group study. J Clin Oncol. 37:1380–1390. 2019.PubMed/NCBI View Article : Google Scholar |
