Efficacy and safety of pressurized intraperitoneal aerosol chemotherapy (PIPAC) in ovarian cancer: a systematic review of current evidence.
Ovarian cancer
PIPAC
Peritoneal carcinomatosis
Pressurized intraperitoneal aerosol chemotherapy
Journal
Archives of gynecology and obstetrics
ISSN: 1432-0711
Titre abrégé: Arch Gynecol Obstet
Pays: Germany
ID NLM: 8710213
Informations de publication
Date de publication:
15 Jun 2024
15 Jun 2024
Historique:
received:
25
01
2024
accepted:
04
06
2024
medline:
16
6
2024
pubmed:
16
6
2024
entrez:
15
6
2024
Statut:
aheadofprint
Résumé
PIPAC is a recent approach for intraperitoneal chemotherapy with promising results for patients with peritoneal carcinomatosis. A systematic review was conducted to assess current evidence on the efficacy and outcomes of PIPAC in patients affected by ovarian cancer. The study adhered to the PRISMA guidelines. PubMed, Google Scholar and ClinicalTrials.gov were searched up to December 2023. Studies reporting data on patients with OC treated with PIPAC were included in the qualitative analysis. Twenty-one studies and six clinical trials with 932 patients who underwent PIPAC treatment were identified. The reported first access failure was 4.9%. 89.8% of patients underwent one, 60.7% two and 40% received three or more PIPAC cycles. Pathological tumour response was objectivated in 13 studies. Intra-operative complications were reported in 11% of women and post-operative events in 11.5% with a 0.82% of procedure-related mortality. Quality of life scores have been consistently stable or improved during the treatment time. The percentage of OC patients who became amenable for cytoreductive surgery due to the good response after PIPAC treatment for palliative purposes is reported to be 2.3%. The results showed that PIPAC is safe and effective for palliative purposes, with a good pathological tumour response and quality of life. Future prospective studies would be needed to explore the role of this treatment in different stages of the disease, investigating a paradigm shift towards the use of PIPAC with curative intent for women who are not eligible for primary cytoreductive surgery.
Sections du résumé
BACKGROUND
BACKGROUND
PIPAC is a recent approach for intraperitoneal chemotherapy with promising results for patients with peritoneal carcinomatosis. A systematic review was conducted to assess current evidence on the efficacy and outcomes of PIPAC in patients affected by ovarian cancer.
METHODS
METHODS
The study adhered to the PRISMA guidelines. PubMed, Google Scholar and ClinicalTrials.gov were searched up to December 2023. Studies reporting data on patients with OC treated with PIPAC were included in the qualitative analysis.
RESULTS
RESULTS
Twenty-one studies and six clinical trials with 932 patients who underwent PIPAC treatment were identified. The reported first access failure was 4.9%. 89.8% of patients underwent one, 60.7% two and 40% received three or more PIPAC cycles. Pathological tumour response was objectivated in 13 studies. Intra-operative complications were reported in 11% of women and post-operative events in 11.5% with a 0.82% of procedure-related mortality. Quality of life scores have been consistently stable or improved during the treatment time. The percentage of OC patients who became amenable for cytoreductive surgery due to the good response after PIPAC treatment for palliative purposes is reported to be 2.3%.
CONCLUSION
CONCLUSIONS
The results showed that PIPAC is safe and effective for palliative purposes, with a good pathological tumour response and quality of life. Future prospective studies would be needed to explore the role of this treatment in different stages of the disease, investigating a paradigm shift towards the use of PIPAC with curative intent for women who are not eligible for primary cytoreductive surgery.
Identifiants
pubmed: 38879697
doi: 10.1007/s00404-024-07586-z
pii: 10.1007/s00404-024-07586-z
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fondation de l'Avenir pour la Recherche Médicale Appliquée
ID : ANR-10-IAHU-02
Informations de copyright
© 2024. The Author(s).
Références
Bray F, Sankila R, Ferlay J, Parkin DM (2002) Estimates of cancer incidence and mortality in Europe in 1995. Eur J Cancer Oxf Engl 1990 38(1):99–166
Marchetti C, Rosati A, De Felice F, Boccia SM, Vertechy L, Pavone M et al (2021) Optimizing the number of cycles of neoadjuvant chemotherapy in advanced epithelial ovarian carcinoma: a propensity-score matching analysis. Gynecol Oncol 163(1):29–35
pubmed: 34312003
doi: 10.1016/j.ygyno.2021.07.025
Ghirardi V, Fagotti A, Scambia G (2023) Laparoscopic selection for surgery in epithelial ovarian cancer. a short review. Facts Views Vis ObGyn 15(1):25–28
pubmed: 37010331
pmcid: 10392116
doi: 10.52054/FVVO.15.1.060
Pujade-Lauraine E, Ledermann JA, Selle F, Gebski V, Penson RT, Oza AM et al (2017) Olaparib tablets as maintenance therapy in patients with platinum-sensitive, relapsed ovarian cancer and a BRCA1/2 mutation (SOLO2/ENGOT-Ov21): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol 18(9):1274–1284
pubmed: 28754483
doi: 10.1016/S1470-2045(17)30469-2
Du Bois A, Vergote I, Ferron G, Reuss A, Meier W, Greggi S et al (2017) Randomized controlled phase III study evaluating the impact of secondary cytoreductive surgery in recurrent ovarian cancer: AGO DESKTOP III/ENGOT ov20. J Clin Oncol 35(15):5501–5501
doi: 10.1200/JCO.2017.35.15_suppl.5501
Hanker LC, Loibl S, Burchardi N, Pfisterer J, Meier W, Pujade-Lauraine E et al (2012) The impact of second to sixth line therapy on survival of relapsed ovarian cancer after primary taxane/platinum-based therapy. Ann Oncol 23(10):2605–2612
pubmed: 22910840
doi: 10.1093/annonc/mds203
Ghirardi V, Trozzi R, Scambia G, Fagotti A (2023) Current and future trials about HIPEC in ovarian cancer. Bull Cancer (Paris) S0007–4551(23):00082–00086
Di Giorgio A, Abatini C, Attalla El Halabieh M, Vita E, Vizzielli G, Gallotta V et al (2019) From palliation to cure: PIPAC for peritoneal malignancies. Minerva Med 110(4):385–398
pubmed: 31081306
doi: 10.23736/S0026-4806.19.06081-6
van Driel WJ, Koole SN, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RHM et al (2018) Hyperthermic intraperitoneal chemotherapy in ovarian cancer. N Engl J Med 378(3):230–240
pubmed: 29342393
doi: 10.1056/NEJMoa1708618
Furet E, Chéreau E, Lambaudie E, Bannier M, Houvenaeghel G (2013) Feasibility, morbidity and survival of surgery combined with HIPEC in the management of recurrent ovarian cancer. Gynecol Obstet Fertil 41(9):493–498
pubmed: 23972918
doi: 10.1016/j.gyobfe.2013.07.011
Koole S, van Stein R, Sikorska K, Barton D, Perrin L, Brennan D et al (2020) 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(6):888–892
pubmed: 32205449
pmcid: 8202725
doi: 10.1136/ijgc-2020-001231
Cianci S, Ronsini C, Vizzielli G, Tropea A, Biondi A, Scambia G et al (2019) Cytoreductive surgery followed by HIPEC repetition for secondary ovarian cancer recurrence. Updat Surg 71(2):389–394
doi: 10.1007/s13304-018-0600-y
Solass W, Kerb R, Mürdter T, Giger-Pabst U, Strumberg D, Tempfer C et al (2014) Intraperitoneal chemotherapy of peritoneal carcinomatosis using pressurized aerosol as an alternative to liquid solution: first evidence for efficacy. Ann Surg Oncol 21(2):553–559
pubmed: 24006094
doi: 10.1245/s10434-013-3213-1
Khosrawipour V, Khosrawipour T, Kern AJP, Osma A, Kabakci B, Diaz-Carballo D et al (2016) Distribution pattern and penetration depth of doxorubicin after pressurized intraperitoneal aerosol chemotherapy (PIPAC) in a postmortem swine model. J Cancer Res Clin Oncol 142(11):2275–2280
pubmed: 27590613
doi: 10.1007/s00432-016-2234-0
Hübner M, Grass F, Teixeira-Farinha H, Pache B, Mathevet P, Demartines N (2017) Pressurized intraperitoneal aerosol chemotherapy—practical aspects. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 43(6):1102–1109
Blanco A, Giger-Pabst U, Solass W, Zieren J, Reymond MA (2013) Renal and hepatic toxicities after pressurized intraperitoneal aerosol chemotherapy (PIPAC). Ann Surg Oncol 20(7):2311–2316
pubmed: 23377563
pmcid: 3675273
doi: 10.1245/s10434-012-2840-2
Grass F, Vuagniaux A, Teixeira-Farinha H, Lehmann K, Demartines N, Hübner M (2017) Systematic review of pressurized intraperitoneal aerosol chemotherapy for the treatment of advanced peritoneal carcinomatosis. Br J Surg 104(6):669–678
pubmed: 28407227
doi: 10.1002/bjs.10521
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097
pubmed: 19621072
pmcid: 2707599
doi: 10.1371/journal.pmed.1000097
Basch E, Reeve BB, Mitchell SA, Clauser SB, Minasian LM, Dueck AC et al (2014) Development of the national cancer institute’s patient-reported outcomes version of the common terminology criteria for adverse events (PRO-CTCAE). J Natl Cancer Inst 106(9):dju244
pubmed: 25265940
pmcid: 4200059
doi: 10.1093/jnci/dju244
Elzarkaa AA, Shaalan W, Elemam D, Mansour H, Melis M, Malik E et al (2018) Peritoneal cancer index as a predictor of survival in advanced stage serous epithelial ovarian cancer: a prospective study. J Gynecol Oncol 29(4):e47
pubmed: 29770618
pmcid: 5981099
doi: 10.3802/jgo.2018.29.e47
Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L et al (2000) New guidelines to evaluate the response to treatment in solid tumors European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92(3):205–216
pubmed: 10655437
doi: 10.1093/jnci/92.3.205
Solass W, Sempoux C, Detlefsen S, Carr NJ, Bibeau F (2016) Peritoneal sampling and histological assessment of therapeutic response in peritoneal metastasis: proposal of the Peritoneal Regression Grading Score (PRGS). Pleura Peritoneum 1(2):99–107
pubmed: 30911613
pmcid: 6328069
doi: 10.1515/pp-2016-0011
Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ et al (1993) The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 85(5):365–376
pubmed: 8433390
doi: 10.1093/jnci/85.5.365
Brazier J, Roberts J, Deverill M (2002) The estimation of a preference-based measure of health from the SF-36. J Health Econ 21(2):271–292
pubmed: 11939242
doi: 10.1016/S0167-6296(01)00130-8
Tempfer CB, Winnekendonk G, Solass W, Horvat R, Giger-Pabst U, Zieren J et al (2015) Pressurized intraperitoneal aerosol chemotherapy in women with recurrent ovarian cancer: a phase 2 study. Gynecol Oncol 137(2):223–228
pubmed: 25701703
doi: 10.1016/j.ygyno.2015.02.009
Tempfer CB, Solass W, Reymond MA (2014) Pressurized intraperitoneal chemotherapy (PIPAC) in women with gynecologic malignancies: a review. Wien Med Wochenschr 164(23–24):519–528
pubmed: 25249025
doi: 10.1007/s10354-014-0312-y
Tempfer CB (2015) Pressurized intraperitoneal aerosol chemotherapy as an innovative approach to treat peritoneal carcinomatosis. Med Hypotheses 85(4):480–484
pubmed: 26277656
doi: 10.1016/j.mehy.2015.07.001
Tempfer CB, Hartmann F, Hilal Z, Rezniczek GA (2017) Intraperitoneal cisplatin and doxorubicin as maintenance chemotherapy for unresectable ovarian cancer: a case report. BMC Cancer 17(1):26
pubmed: 28061769
pmcid: 5216537
doi: 10.1186/s12885-016-3004-8
Giger-Pabst U, Solass W, Buerkle B, Reymond MA, Tempfer CB (2015) Low-dose pressurized intraperitoneal aerosol chemotherapy (PIPAC) as an alternative therapy for ovarian cancer in an octogenarian patient. Anticancer Res 35(4):2309–2314
pubmed: 25862894
Tempfer CB, Giger-Pabst U, Seebacher V, Petersen M, Dogan A, Rezniczek GA (2018) A phase I, single-arm, open-label, dose escalation study of intraperitoneal cisplatin and doxorubicin in patients with recurrent ovarian cancer and peritoneal carcinomatosis. Gynecol Oncol 150(1):23–30
pubmed: 29743140
doi: 10.1016/j.ygyno.2018.05.001
Odendahl K, Solass W, Demtröder C, Giger-Pabst U, Zieren J, Tempfer C et al (2015) Quality of life of patients with end-stage peritoneal metastasis treated with Pressurized intraperitoneal aerosol chemotherapy (PIPAC). Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 41(10):1379–1385
Somashekhar SP, Rajagopal AK, Zaveri SS, Chandrashekhar RK, Rauthan A, Rakshit SH (2018) First Indian study on pressurized intraperitoneal aerosol chemotherapy (PIPAC) procedure for advanced peritoneal carcinomatosis secondary to epithelial ovarian cancer. Indian J Gynecol Oncol 16(2):25
doi: 10.1007/s40944-018-0193-x
Teixeira Farinha H, Grass F, Kefleyesus A, Achtari C, Romain B, Montemurro M et al (2017) Impact of pressurized intraperitoneal aerosol chemotherapy on quality of life and symptoms in patients with peritoneal carcinomatosis: a retrospective cohort study. Gastroenterol Res Pract 2017:1–10
doi: 10.1155/2017/4596176
Robella M, Vaira M, De Simone M (2016) Safety and feasibility of pressurized intraperitoneal aerosol chemotherapy (PIPAC) associated with systemic chemotherapy: an innovative approach to treat peritoneal carcinomatosis. World J Surg Oncol 14(1):128
pubmed: 27125996
pmcid: 4850728
doi: 10.1186/s12957-016-0892-7
Alyami M, Gagniere J, Sgarbura O, Cabelguenne D, Villeneuve L, Pezet D et al (2017) Multicentric initial experience with the use of the pressurized intraperitoneal aerosol chemotherapy (PIPAC) in the management of unresectable peritoneal carcinomatosis. Eur J Surg Oncol 43(11):2178–2183
pubmed: 28964609
doi: 10.1016/j.ejso.2017.09.010
Kurtz F, Struller F, Horvath P, Solass W, Bösmüller H, Königsrainer A et al (2018) Feasibility, safety, and efficacy of pressurized intraperitoneal aerosol chemotherapy (PIPAC) for peritoneal metastasis: a registry study. Gastroenterol Res Pract 24(2018):1–8
doi: 10.1155/2018/2743985
Larbre V, Alyami M, Mercier F, Vantard N, Bonnefoy I, Opsomer MA et al (2018) No renal toxicity after repeated treatment with pressurized intraperitoneal aerosol chemotherapy (PIPAC) in patients with unresectable peritoneal metastasis. Anticancer Res 38(12):6869–6875
pubmed: 30504403
doi: 10.21873/anticanres.13062
Siebert M, Alyami M, Mercier F, Gallice C, Villeneuve L, Laplace N et al (2021) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) in association with systemic chemotherapy and bevacizumab, evaluation of safety and feasibility. A single center comparative study. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol. 47(1):139–142
Sgarbura O, Hübner M, Alyami M, Eveno C, Gagnière J, Pache B et al (2019) Oxaliplatin use in pressurized intraperitoneal aerosol chemotherapy (PIPAC) is safe and effective: a multicenter study. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 45(12):2386–2391
Ceribelli C, Debs T, Chevallier A, Piche MA, Bereder JM (2020) Initial experience of pressurized intraperitoneal aerosol chemotherapy (PIPAC) in a French hyperthermic intraperitoneal chemotherapy (HIPEC) expert center. Surg Endosc 34(6):2803–2806
pubmed: 32166545
doi: 10.1007/s00464-020-07488-6
De Simone M, Vaira M, Argenziano M, Berchialla P, Pisacane A, Cinquegrana A et al (2020) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) with oxaliplatin, cisplatin, and doxorubicin in patients with peritoneal carcinomatosis: an open-label, single-arm, phase II clinical trial. Biomedicines 8(5):102
pubmed: 32365877
pmcid: 7277495
doi: 10.3390/biomedicines8050102
Račkauskas R, Baušys A, Lukšta M, Jurgaitis J, Paškonis M, Strupas K (2021) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) for peritoneal malignancy: initial experience of the first program in the Baltic countries. World J Surg Oncol 19(1):236
pubmed: 34376191
pmcid: 8356452
doi: 10.1186/s12957-021-02357-5
Hübner M, Teixeira Farinha H, Grass F, Wolfer A, Mathevet P, Hahnloser D et al (2017) Feasibility and safety of pressurized intraperitoneal aerosol chemotherapy for peritoneal carcinomatosis: a retrospective cohort study. Gastroenterol Res Pract 2017:1–7
doi: 10.1155/2017/6852749
Mehta S, Kammar P, Patel A, Goswami G, Shaikh S, Sukumar V et al (2022) Feasibility and safety of taxane-PIPAC in patients with peritoneal malignancies-a retrospective bi-institutional study. Indian J Surg Oncol 7:1–9
Vizzielli G, Giudice MT, Nardelli F, Costantini B, Salutari V, Inzani FS et al (2023) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) applied to platinum-resistant recurrence of ovarian tumor: a single-institution experience (ID: PARROT trial). Ann Surg Oncol 31(2):1207–1216
pubmed: 38099993
pmcid: 10761392
doi: 10.1245/s10434-023-14648-0
Taliento C, Restaino S, Scutiero G, Arcieri M, Bernardi G, Martinello R et al (2023) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) with cisplatin and doxorubicin in patients with ovarian cancer: a systematic review. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 49(12):107250
Markman M (2003) Intraperitoneal antineoplastic drug delivery: rationale and results. Lancet Oncol 4(5):277–283
pubmed: 12732164
doi: 10.1016/S1470-2045(03)01074-X
Nadiradze G, Giger-Pabst U, Zieren J, Strumberg D, Solass W, Reymond MA (2016) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) with low-dose cisplatin and doxorubicin in gastric peritoneal metastasis. J Gastrointest Surg Off J Soc Surg Aliment Tract 20(2):367–373
doi: 10.1007/s11605-015-2995-9
Alyami M, Bonnot PE, Mercier F, Laplace N, Villeneuve L, Passot G et al (2021) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) for unresectable peritoneal metastasis from gastric cancer. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 47(1):123–127
Al-Batran SE, Homann N, Pauligk C, Illerhaus G, Martens UM, Stoehlmacher J et al (2017) Effect of neoadjuvant chemotherapy followed by surgical resection on survival in patients with limited metastatic gastric or gastroesophageal junction cancer: the AIO-FLOT3 trial. JAMA Oncol 3(9):1237–1244
pubmed: 28448662
pmcid: 5824287
doi: 10.1001/jamaoncol.2017.0515
Franko J, Shi Q, Meyers JP, Maughan TS, Adams RA, Seymour MT et al (2016) Prognosis of patients with peritoneal metastatic colorectal cancer given systemic therapy: an analysis of individual patient data from prospective randomised trials from the analysis and research in cancers of the digestive system (ARCAD) database. Lancet Oncol 17(12):1709–1719
pubmed: 27743922
doi: 10.1016/S1470-2045(16)30500-9
Miura JT, Johnston FM, Gamblin TC, Turaga KK (2014) Current trends in the management of malignant peritoneal mesothelioma. Ann Surg Oncol 21(12):3947–3953
pubmed: 24841356
doi: 10.1245/s10434-014-3803-6
Girshally R, Demtröder C, Albayrak N, Zieren J, Tempfer C, Reymond MA (2016) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) as a neoadjuvant therapy before cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. World J Surg Oncol 14(1):253
pubmed: 27678344
pmcid: 5039790
doi: 10.1186/s12957-016-1008-0
Giger-Pabst U, Tempfer CB (2018) How to perform safe and technically optimized pressurized intraperitoneal aerosol chemotherapy (PIPAC): experience after a consecutive series of 1200 procedures. J Gastrointest Surg 22(12):2187–2193
pubmed: 30132291
doi: 10.1007/s11605-018-3916-5