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Pharmacological considerations regarding intraoperative hyperthermic intraperitoneal chemotherapy for ovarian cancer
1Department of Surgical Oncology, Medical School of Crete University Hospital, 71110 Heraklion, Greece
2Department of Biochemistry, Medical School of Crete, 71013 Heraklion, Greece
DOI: 10.31083/j.ejgo4205151 Vol.42,Issue 5,October 2021 pp.1018-1028
Submitted: 09 August 2021 Accepted: 07 September 2021
Published: 15 October 2021
*Corresponding Author(s): Eelco de Bree E-mail: debree@edu.uoc.gr
Since ovarian cancer is limited to the peritoneal cavity for a prolonged period during the disease course, intraperitoneal chemotherapy seems a rational treatment option for residual peritoneal disease after cytoreductive surgery. Intraperitoneal when compared with intravenous chemotherapy exhibits a clear pharmacokinetic benefit. Performing intraperitoneal chemotherapy under hyperthermic conditions, as in intraoperative hyperthermic intraperitoneal chemotherapy (HIPEC), may enhance its therapeutic efficacy. Herein, the pharmacological aspects of (hyperthermic) intraperitoneal chemotherapy are discussed, including pharmacokinetics, drug penetration depth into the tumour, drug characteristics, optimal drug choice and the role of hyperthermia. Further clinical pharmacological studies are needed to appraise the optimal drug regimen for HIPEC in patients with primary and recurrent ovarian can-cer. Development of new drugs and drug formulations may further improve the efficacy of HIPEC in the future.
Ovarian cancer; Intraperitoneal chemotherapy; HIPEC; Hyperthermia; Drug choice; Pharmacokinetics
Eelco de Bree,Dimosthenis Michelakis,Hara Polioudaki,Elisabeth Anagnostopoulou,Panayiotis A. Theodoropoulos. Pharmacological considerations regarding intraoperative hyperthermic intraperitoneal chemotherapy for ovarian cancer. European Journal of Gynaecological Oncology. 2021. 42(5);1018-1028.
[1] Weisberger AS, Levine B, Storaasli JP. Use of nitrogen mustard in treatment of serous effusions of neoplastic origin. Journal of the American Medical Association. 1955; 159: 1704–1707.
[2] de Bree E, Tsiftsis DD. Principles of perioperative intraperitoneal chemotherapy for peritoneal carcinomatosis. Recent Results in Cancer Research. Fortschritte Der Krebsforschung. Progres Dans Les Recherches Sur Le Cancer. 2007; 169: 39–51.
[3] de Bree E, Michelakis D. An overview and update of hyperthermic intraperitoneal chemotherapy in ovarian cancer. Expert Opinion on Pharmacotherapy. 2020; 21: 1479–1492.
[4] Spiliotis J, Halkia E, Lianos E, Kalantzi N, Grivas A, Efstathiou E, et al. Cytoreductive surgery and HIPEC in recurrent epithelial ovarian cancer: a prospective randomized phase III study. Annals of Surgical Oncology. 2015; 22: 1570–1575.
[5] van Driel WJ, Koole SN, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RHM, et al. Hyperthermic intraperitoneal chemotherapy in ovarian cancer. The New England Journal of Medicine. 2018; 378: 230–240.
[6] de Bree E, Tsiftsis DD. Experimental and pharmacokinetic studies in intraperitoneal chemotherapy: from laboratory bench to bedside. Recent Results in Cancer Research. Fortschritte Der Krebsforschung. Progres Dans Les Recherches Sur Le Cancer. 2007; 169: 53–73.
[7] de Bree E, Michelakis D, Stamatiou D, Romanos J, Zoras O. Pharmacological principles of intraperitoneal and bidirectional chemotherapy. Pleura and Peritoneum. 2017; 2: 47–62.
[8] Jacquet P, Sugarbaker PH. Peritoneal-plasma barrier. Cancer Treatment and Research. 1996; 82: 53–63.
[9] Flessner MF. The transport barrier in intraperitoneal therapy. American Journal of Physiology. Renal Physiology. 2005; 288: F433–F442.
[10] Van der Speeten K, Stuart OA, Sugarbaker PH. Pharmacokinetics and pharmacodynamics of perioperative cancer chemotherapy in peritoneal surface malignancy. The Cancer Journal. 2009; 15: 216–224.
[11] Speyer JL, Sugarbaker PH, Collins JM, Dedrick RL, Klecker RW Jr, Myers CE. Portal levels and hepatic clearance of 5-fluorouracil after intraperitoneal administration in humans. Cancer Research. 1981; 41: 1916–1922.
[12] Lindnér P, Heath DD, Shalinsky DR, Howell SB, Naredi P, Haf-ström L. Regional lymphatic drug exposure following intraperitoneal administration of 5-fluorouracil, carboplatin, and etoposide. Surgical Oncology. 1993; 2: 105–112.
[13] Ozols RF, Locker GY, Doroshow JH, Grotzinger KR, Myers CE, Young RC. Pharmacokinetics of adriamycin and tissue penetration in murine ovarian cancer. Cancer Research. 1979; 39: 3209–3214.
[14] McVie JG, Dikhoff T, Van der Heide J, Dubbelman R, ten Bokkel Huinink WW. Tissue concentration of platinum after intraperitoneal cisplatinum administration in patients. Proceedings of the American Association for Cancer Research. 1985; 26: 162.
[15] Los G, Verdegaal EM, Mutsaers PH, McVie JG. Penetration of carboplatin and cisplatin into rat peritoneal tumor nodules after intraperitoneal chemotherapy. Cancer Chemotherapy and Pharma-cology. 1991; 28: 159–165.
[16] Fujimoto S, Takahashi M, Kobayashi K, Nagano K, Kure M, Mutoh T, et al. Cytohistologic assessment of antitumor effects of intraperitoneal hyperthermic perfusion with mitomycin C for patients with gastric cancer with peritoneal metastasis. Cancer. 1992; 70: 2754–2760.
[17] Panteix G, Guillaumont M, Cherpin L, Cuichard J, Gilly FN, Carry PY, et al. Study of the pharmakokinetics of mitomycin C in humans during intraperitoneal chemohyperthermia with special mention of the concentration in local tissues. Oncology. 1993; 50: 366–370.
[18] van de Vaart PJ, van der Vange N, Zoetmulder FA, van Goethem AR, van Tellingen O, ten Bokkel Huinink WW, et al. Intraperi-toneal cisplatin with regional hyperthermia in advanced ovarian cancer: pharmacokinetics and cisplatin-DNA adduct formation in patients and ovarian cancer cell lines. European Journal of Cancer. 1998; 34: 148–154.
[19] Collins JM, Dedrick RL, Flessner MF, Guarino AM. Concentration-dependent disappearance of fluorouracil from peritoneal fluid in the rat: experimental observations and distributed modeling. Journal of Pharmaceutical Sciences. 1982; 71: 735–738.
[20] Steuperaert M, Debbaut C, Segers P, Ceelen W. Modelling drug transport during intraperitoneal chemotherapy. Pleura and Peritoneum. 2017; 2: 73–83.
[21] Steuperaert M, Falvo D’Urso Labate G, Debbaut C, De Wever O, Vanhove C, Ceelen W, et al. Mathematical modeling of intraperitoneal drug delivery: simulation of drug distribution in a single tumor nodule. Drug Delivery. 2017; 24: 491–501.
[22] Steuperaert M, Debbaut C, Carlier C, De Wever O, Descamps B, Vanhove C, et al. A 3D CFD model of the interstitial fluid pressure and drug distribution in heterogeneous tumor nodules during intraperitoneal chemotherapy. Drug Delivery. 2019; 26: 404–415.
[23] Ceelen WP, Flessner MF. Intraperitoneal therapy for peritoneal tumors: biophysics and clinical evidence. Nature Reviews. Clinical Oncology. 2010; 7: 108–115.
[24] Michalakis J, Georgatos SD, de Bree E, Polioudaki H, Romanos J, Georgoulias V, et al. Short-term exposure of cancer cells to micromolar doses of paclitaxel, with or without hyperthermia, induces long-term inhibition of cell proliferation and cell death in vitro. Annals of Surgical Oncology. 2007; 14: 1220–1228.
[25] Rupniak HT, Whelan RDH, Hill BT. Concentration and time-dependent inter-relationships for antitumour drug cytotoxicities against tumour cells in vitro. International Journal of Cancer. 1983; 32: 7–12.
[26] Alberts DS, Young L, Mason N, Salmon SE. In vitro evaluation of anticancer drugs against ovarian cancer at concentrations achievable by intraperitoneal administration. Seminars in Oncology. 1985; 12: 38–42.
[27] Link K, Leder G, Pillasch J, Butzer U, Staib L, Kornmann M, et al. In vitro concentration response studies and in vitro phase II tests as the experimental basis for regional chemotherapeutic protocols. Seminars in Surgical Oncology. 1998; 14: 189–201.
[28] Muller M, Chérel M, Dupré P, Gouard S, Collet M, Classe J. The cytotoxic effect of combined hyperthermia and taxane chemotherapy on ovarian cancer cells: results of an in vitro study. European Surgical Research. Europaische Chirurgische Forschung. Recherches Chirurgicales Europeennes. 2012; 48: 55–63.
[29] Chua TC, Yan TD, Saxena A, Morris DL. Should the treatment of peritoneal carcinomatosis by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy still be regarded as a highly morbid procedure?: a systematic review of morbidity and mortality. Annals of Surgery. 2009; 249: 900–907.
[30] Hotouras A, Desai D, Bhan C, Murphy J, Lampe B, Sugarbaker PH. Heated intraperitoneal chemotherapy (HIPEC) for patients with recurrent ovarian cancer: a systematic literature review. Interna-tional Journal of Gynecologic Cancer. 2016; 26: 661–670.
[31] Wang Y, Ren F, Chen P, Liu S, Song Z, Ma X. Effects of CytoRe-ductive surgery plus hyperthermic IntraPEritoneal chemotherapy (HIPEC) versus CytoReductive surgery for ovarian cancer patients: a systematic review and meta-analysis. European Journal of Surgical Oncology. 2019; 45: 301–309.
[32] Hildebrandt B, Wust P, Ahlers O, Dieing A, Sreenivasa G, Kerner T, et al. The cellular and molecular basis of hyperthermia. Critical Reviews in Oncology/Hematology. 2002; 43: 33–56.
[33] de Bree E. Optimal drugs for HIPEC in different tumors. Journal of B.U.on. 2015; 20: S40–S46.
[34] Urano M, Ling CC. Thermal enhancement of melphalan and oxaliplatin cytotoxicity in vitro. International Journal of Hyperthermia. 2002; 18: 307–315.
[35] Takemoto M, Kuroda M, Urano M, Nishimura Y, Kawasaki S, Kato H, et al. The effect of various chemotherapeutic agents given with mild hyperthermia on different types of tumours. International Journal of Hyperthermia. 2003; 19: 193–203.
[36] Murata S, Yamamoto H, Shimizu T, Naitoh H, Yamaguchi T, Kaida S, et al. 5-fluorouracil combined with cisplatin and mitomycin C as an optimized regimen for hyperthermic intraperi-toneal chemotherapy in gastric cancer. Journal of Surgical Oncol-ogy. 2018; 117: 671–677.
[37] Urano M, Kuroda M, Nishimura Y. For the clinical application of thermochemotherapy given at mild temperatures. International Journal of Hyperthermia. 1999; 15: 79–107.
[38] Lepock JR. How do cells respond to their thermal environment?International Journal of Hyperthermia. 2005; 21: 681–687.
[39] Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. International Journal of Hyperthermia. 2014; 30: 531–539.
[40] Yarmolenko PS, Moon EJ, Landon C, Manzoor A, Hochman DW, Viglianti BL, et al. Thresholds for thermal damage to normal tissues: an update. International Journal of Hyperthermia. 2011; 27: 320–343.
[41] de Bree E, Katsougkri D, Polioudaki H, Tsangaridou E, Michelakis D, Zoras O, et al. Hyperthermia during intraperitoneal chemotherapy with paclitaxel or docetaxel for ovarian cancer: is there any benefit? Anticancer Research. 2020; 40: 6769–6780.
[42] Bear AS, Kennedy LC, Young JK, Perna SK, Mattos Almeida JP, Lin AY, et al. Elimination of metastatic melanoma using gold nanoshell-enabled photothermal therapy and adoptive T cell transfer. PLoS ONE. 2013; 8: e69073.
[43] Kepenekian V, Aloy M, Magné N, Passot G, Armandy E, Decullier E, et al. Impact of hyperthermic intraperitoneal chemotherapy on Hsp27 protein expression in serum of patients with peritoneal carcinomatosis. Cell Stress & Chaperones. 2013; 18: 623–630.
[44] Tu Y, Tian Y, Wu Y, Cui S. Clinical significance of heat shock proteins in gastric cancer following hyperthermia stress: Indications for hyperthermic intraperitoneal chemoperfusion therapy. Oncology Letters. 2018; 15: 9385–9391.
[45] Pelz JOW, Vetterlein M, Grimmig T, Kerscher AG, Moll E, Lazar-iotou M, et al. Hyperthermic intraperitoneal chemotherapy in patients with peritoneal carcinomatosis: role of heat shock proteins and dissecting effects of hyperthermia. Annals of Surgical Oncol-ogy. 2013; 20: 1105–1113.
[46] Grimmig T, Moll E, Kloos K, Thumm R, Moench R, Callies S, et al. Upregulated heat shock proteins after hyperthermic chemotherapy point to induced cell survival mechanisms in affected tumor cells from peritoneal carcinomatosis. Cancer Growth and Metas-tasis. 2017; 10: 1179064417730559.
[47] Cesna V, Sukovas A, Jasukaitiene A, Silkuniene G, Paskauskas S, Dambrauskas Z, et al. Stimulated upregulation of HO-1 is associ-ated with inadequate response of gastric and ovarian cancer cell lines to hyperthermia and cisplatin treatment. Oncology Letters. 2019; 18: 1961–1968.
[48] Lianos GD, Alexiou GA, Mangano A, Mangano A, Rausei S, Boni L, et al. The role of heat shock proteins in cancer. Cancer Letters. 2015; 360: 114–118.
[49] Fisher DT, Appenheimer MM, Evans SS. The two faces of IL-6 in the tumor microenvironment. Seminars in Immunology. 2014; 26: 38–47.
[50] Klaver YLB, Hendriks T, Lomme RMLM, Rutten HJT, Bleichrodt RP, de Hingh IHJT. Hyperthermia and intraperitoneal chemotherapy for the treatment of peritoneal carcinomatosis. Annals of Surgery. 2011; 254: 125–130.
[51] Kireeva GS, Bespalov VG, Belyaeva OA, Senchik KY, Stukov AN, Gafton GI, et al. Normothermic and hyperthermic intraperitoneal chemoperfusions with cisplatin to treat advanced ovarian cancer in experimental settings. Pathology Oncology Research. 2017; 23: 459–460.
[52] Bespalov VG, Alvovsky IK, Tochilnikov GV, Stukov AN, Vyshin-skaya EA, Semenov AL, et al. Comparative efficacy evaluation of catheter intraperitoneal chemotherapy, normothermic and hyper-thermic chemoperfusion in a rat model of ascitic ovarian cancer. International Journal of Hyperthermia. 2018; 34: 545–550.
[53] Li S, Zhang Y, Sun J, Hua Y, Wu P. Safe temperature range for intraoperative and early postoperative continuous hyperthermic intraperitoneal perfusion in a swine model of experimental distal gastrectomy with Billroth II reconstruction. Journal of Transla-tional Medicine. 2013; 11: 181.
[54] Kanellos D, Pramateftakis MG, Mantzoros I, Zacharakis E, Raptis D, Despoudi K, et al. The effects of the intraperitoneal administration of oxaliplatin and 5-FU on the healing of colonic anastomoses: an experimental study. Techniques in Coloproctology. 2011; 15: S111–S115.
[55] Shimizu T, Maeta M, Koga S. Influence of local hyperthermia on the healing of small intestinal anastomoses in the rat. The British Journal of Surgery. 1991; 78: 57–59.
[56] Dokladny K, Zuhl MN, Moseley PL. Intestinal epithelial barrier function and tight junction proteins with heat and exercise. Journal of Applied Physiology. 2016; 120: 692–701.
[57] Coccolini F, Corbella D, Finazzi P, Brambillasca P, Benigni A, Prussiani V, et al. Time course of cytokines, hemodynamic and metabolic parameters during hyperthermic intraperitoneal chemotherapy. Minerva Anestesiologica. 2016; 82: 310–319.
[58] Tsiftsis D, de Bree E, Romanos J, Petrou A, Sanidas E, Askoxy-lakis J, et al. Peritoneal expansion by artificially produced ascites during perfusion chemotherapy. Archives of Surgery. 1999; 134: 545–549.
[59] Gremonprez F, Gossye H, Ceelen W. Use of hyperthermia versus normothermia during intraperitoneal chemoperfusion with oxaliplatin for colorectal peritoneal carcinomatosis: a propensity score matched analysis. European Journal of Surgical Oncology. 2019; 45: 366–370.
[60] de Bree E, Helm CW. Hyperthermic intraperitoneal chemotherapy in ovarian cancer: rationale and clinical data. Expert Review of Anticancer Therapy. 2012; 12: 895–911.
[61] Morales-Soriano R, Esteve-Pérez N, Segura-Sampedro JJ, Cascales-Campos P, Barrios P. Current practice in cytoreductive surgery and HIPEC for metastatic peritoneal disease: Spanish multicentric survey. European Journal of Surgical Oncology. 2018; 44: 228–236.
[62] Cesna V, Sukovas A, Jasukaitiene A, Naginiene R, Barauskas G, Dambrauskas Z, et al. Narrow line between benefit and harm: Additivity of hyperthermia to cisplatin cytotoxicity in different gastrointestinal cancer cells. World Journal of Gastroenterology. 2018; 24: 1072–1083.
[63] Sukovas A, Cesna V, Jasukaitiene A, Barauskas G, Nadisauskiene RJ, Dambrauskas Z, et al. Response of OVCAR-3 cells to cisplatin and hyperthermia: does hyperthermia really matter? Anticancer Research. 2017; 37: 5011–5018.
[64] Gómez-Ruiz ÁJ, González-Gil A, Gil J, Alconchel F, Navarro-Barrios Á, Gil-Gómez E, et al. Acute renal disease in patients with ovarian peritoneal carcinomatosis treated with cytoreduction and HIPEC: the influence of surgery and the cytostatic agent used. Lan-genbeck’s Archives of Surgery. 2021. (in press)
[65] Ye J, Ren Y, Wei Z, Peng J, Chen C, Song W, et al. Nephrotoxicity and long-term survival investigations for patients with peritoneal carcinomatosis using hyperthermic intraperitoneal chemotherapy with cisplatin: a retrospective cohort study. Surgical Oncology. 2018; 27: 456–461.
[66] Liesenfeld LF, Wagner B, Hillebrecht HC, Brune M, Eckert C, Klose J, et al. HIPEC-induced acute kidney injury: a retrospective clinical study and preclinical model. Annals of Surgical Oncology. 2021. (in press)
[67] Dickey DT, Wu YJ, Muldoon LL, Neuwelt EA. Protection against cisplatin-induced toxicities by N-acetylcysteine and sodium thiosulfate as assessed at the molecular, cellular, and in vivo levels. the Journal of Pharmacology and Experimental Therapeutics. 2005; 314: 1052–1058.
[68] Bouhadjari N, Gabato W, Calabrese D, Msika S, Keita H. Hyper-thermic intraperitoneal chemotherapy with cisplatin: Amifostine prevents acute severe renal impairment. European Journal of Surgical Oncology. 2016; 42: 219–223.
[69] Zaballos M, Power M, Canal-Alonso MI, González-Nicolás MÁ, Vasquez-Jimenez W, Lozano-Lominchar P, et al. Effect of cilastatin on cisplatin-induced nephrotoxicity in patients undergoing hyperthermic intraperitoneal chemotherapy. International Journal of Molecular Sciences. 2021; 22: 1239.
[70] Los G, van Vugt MJ, den Engelse L, Pinedo HM. Effects of temperature on the interaction of cisplatin and carboplatin with cellular DNA. Biochemical Pharmacology. 1993; 46: 1229–1237.
[71] de Bree E, Theodoropoulos PA, Rosing H, Michalakis J, Romanos J, Beijnen JH, et al. Treatment of ovarian cancer using intraperitoneal chemotherapy with taxanes: from laboratory bench to bedside. Cancer Treatment Reviews. 2006; 32: 471–482.
[72] de Bree E, Rosing H, Michalakis J, Romanos J, Relakis K, Theodor-opoulos PA, et al. Intraperitoneal chemotherapy with taxanes for ovarian cancer with peritoneal dissemination. European Journal of Surgical Oncology. 2006; 32: 666–670.
[73] de Bree E, Rosing H, Filis D, Romanos J, Melisssourgaki M, Daskalakis M, et al. Cytoreductive surgery and intraoperative hyperthermic intraperitoneal chemotherapy with paclitaxel: a clinical and pharmacokinetic study. Annals of Surgical Oncology. 2008; 15: 1183–1192.
[74] Kuh H-J, Jang SH, Wientjes MG, Weaver JR, Au JL. Determinants of paclitaxel penetration and accumulation in human solid tumor. The Journal of Pharmacology and Experimental Therapeutics. 1999; 290: 871–880.
[75] Ansaloni L, Coccolini F, Morosi L, Ballerini A, Ceresoli M, Grosso G, et al. Pharmacokinetics of concomitant cisplatin and paclitaxel administered by hyperthermic intraperitoneal chemotherapy to patients with peritoneal carcinomatosis from epithelial ovarian cancer. British Journal of Cancer. 2015; 112: 306–312.
[76] NIH. U.S. National Library of Medicine. ClinicalTrials.gov. Avail-able at: https://clinicaltrials.gov/ (Accessed: 10 July 2021).
[77] Bae JH, Lee JM, Ryu KS, Lee YS, Park YG, Hur SY, et al. Treatment of ovarian cancer with paclitaxel- or carboplatin-based intraperitoneal hyperthermic chemotherapy during secondary surgery. Gynecologic Oncology. 2007; 106: 193–200.
[78] Cascales-Campos P, López-López V, Gil J, Arévalo-Pérez J, Nieto A, Barceló F, et al. Hyperthermic intraperitoneal chemotherapy with paclitaxel or cisplatin in patients with stage III-C/IV ovar-ian cancer. is there any difference? Surgical Oncology. 2016; 25: 164–170.
[79] Coccolini F, Campanati L, Catena F, Ceni V, Ceresoli M, Jimenez Cruz J, et al. Hyperthermic intraperitoneal chemotherapy with cisplatin and paclitaxel in advanced ovarian cancer: a multicenter prospective observational study. Journal of Gynecologic Oncology. 2015; 26: 54.
[80] de Bree E, Rosing H, Beijnen JH, Romanos J, Michalakis J, Georgoulias V, et al. Pharmacokinetic study of docetaxel in intraoperative hyperthermic i.p. chemotherapy for ovarian cancer. Anti-Cancer Drugs. 2003; 14: 103–110.
[81] Van der Speeten K, Stuart OA, Mahteme H, Sugarbaker PH. A pharmacologic analysis of intraoperative intracavitary cancer chemotherapy with doxorubicin. Cancer Chemotherapy and Pharmacology. 2009; 63: 799–805.
[82] Nagaoka S, Kawasaki S, Sasaki K, Nakanishi T. Intracellular up-take, retention and cytotoxic effect of adriamycin combined with hyperthermia in vitro. Japanese Journal of Cancer Research. 1986; 77: 205–211.
[83] Sakaguchi Y, Maehara Y, Emi Y, Kohnoe S, Sugimachi K. Adri-amycin combined with hyperthermia and dipyridamole is cytotoxic both in vitro and in vivo. European Surgical Research. Europaische Chirurgische Forschung. Recherches Chirurgicales Europeennes. 1992; 24: 249–256.
[84] Somashekhar SP, Yethadka R, Kumar C R, Ashwin KR, Zaveri S, Rauthan A. Toxicity profile of chemotherapy agents used in cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal surface malignancies. European Journal of Surgical Oncology. 2020; 46: 577–581.
[85] Salvatorelli E, De Tursi M, Menna P, Carella C, Massari R, Co-lasante A, et al. Pharmacokinetics of pegylated liposomal doxorubicin administered by intraoperative hyperthermic intraperitoneal chemotherapy to patients with advanced ovarian cancer and peritoneal carcinomatosis. Drug Metabolism and Disposition: the Biological Fate of Chemicals. 2012; 40: 2365–2373.
[86] Harrison LE, Bryan M, Pliner L, Saunders T. Phase I trial of pe-gylated liposomal doxorubicin with hyperthermic intraperitoneal chemotherapy in patients undergoing cytoreduction for advanced intra-abdominal malignancy. Annals of Surgical Oncology. 2008; 15: 1407–1413.
[87] Ning S, Macleod K, Abra RM, Huang AH, Hahn GM. Hyperther-mia induces doxorubicin release from long-circulating liposomes and enhances their anti-tumor efficacy. International Journal of Radiation Oncology, Biology, Physics. 1994; 29: 827–834.
[88] Boisen MM, Richard SD, Holtzman MP, Edwards RP, Kelley JL, Choudry MH, et al. Hyperthermic intraperitoneal chemotherapy for epithelial ovarian cancers: is there a role? Journal of Gastrointestinal Oncology. 2016; 7: 10–17.
[89] van Ruth S, Verwaal VJ, Zoetmulder FA. Pharmacokinetics of in-traperitoneal mitomycin C. Surgical Oncology Clinics of North America. 2003; 12: 771–780.
[90] Bijelic L, Sugarbaker PH, Stuart OA. Hyperthermic intraperitoneal chemotherapy with melphalan: a summary of clinical and pharmacological data in 34 patients. Gastroenterology Research and Practice. 2012; 2012: 827534.
[91] Sardi A, Jimenez W, Nieroda C, Sittig M, Shankar S, Gushchin V. Melphalan: a promising agent in patients undergoing cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Annals of Surgical Oncology. 2014; 21: 908–914.
[92] Mahteme H, von Heideman A, Grundmark B, Tholander B, Påhlman L, Glimelius B, et al. Heterogeneous activity of cytotoxic drugs in patient samples of peritoneal carcinomatosis. European Journal of Surgical Oncology. 2008; 34: 547–552.
[93] von Heideman A, Tholander B, Grundmark B, Cajander S, Gerdin E, Holm L, et al. Chemotherapeutic drug sensitivity of primary cultures of epithelial ovarian cancer cells from patients in relation to tumour characteristics and therapeutic outcome. Acta Oncologica. 2014; 53: 242–250.
[94] Bhagwandin S, Naffouje S, Salti G. Utility of chemoresponse assay in patients undergoing cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy. Annals of Surgical Oncology. 2015; 22: 2573–2577.
[95] Kwakman R, de Cuba EM, de Winter JP, de Hingh IH, Delis-van Diemen PM, Tijssen M, et al. Tailoring heated intraperitoneal mitomycin C for peritoneal metastases originating from colorec-tal carcinoma: translational approach to improve survival. British Journal of Cancer. 2015; 112: 851–856.
[96] De Clercq K, Xie F, De Wever O, Descamps B, Hoorens A, Ver-meulen A, et al. Preclinical evaluation of local prolonged release of paclitaxel from gelatin microspheres for the prevention of recurrence of peritoneal carcinomatosis in advanced ovarian cancer. Scientific Reports. 2019; 9: 14881.
[97] Ohta S, Hiramoto S, Amano Y, Emoto S, Yamaguchi H, Ishigami H, et al. Intraperitoneal delivery of cisplatin via a hyaluronan-based nanogel/in situ cross-linkable hydrogel hybrid system for peritoneal dissemination of gastric cancer. Molecular Pharmaceutics. 2017; 14: 3105–3113.
[98] Shariati M, Lollo G, Matha K, Descamps B, Vanhove C, Van de Sande L, et al. Synergy between intraperitoneal aerosolization (PI-PAC) and cancer nanomedicine: cisplatin-loaded polyarginine-hyaluronic acid nanocarriers efficiently eradicate peritoneal metastasis of advanced human ovarian cancer. ACS Applied Materials & Interfaces. 2020; 12: 29024–29036.
[99] Alyami M, Hübner M, Grass F, Bakrin N, Villeneuve L, Laplace N, et al. Pressurised intraperitoneal aerosol chemotherapy: rationale, evidence, and potential indications. The Lancet Oncology. 2019; 20: e368–e377.
[100] Oh S, Paik H, Park SJ, Lee EJ, Kim HS. Pressurized intraperitoneal aerosol chemotherapy for recurrent ovarian, fallopian or primary peritoneal cancer with peritoneal carcinomatosis: a narrative review. Gland Surgery. 2021; 10: 1244–1251.
[101] Ceribelli C, Debs T, Chevallier A, Piche MA, Bereder JM. Initial experience of pressurized intraperitoneal aerosol chemotherapy (PIPAC) in a French hyperthermic intraperitoneal chemotherapy (HIPEC) expert center. Surgical Endoscopy. 2020; 34: 2803–2806.
[102] Tempfer CB, Giger-Pabst U, Seebacher V, Petersen M, Dogan A, Rezniczek GA. A phase i, singlearm, open-label, dose escalation study of intraperitoneal cisplatin and doxorubicin in patients with recurrent ovarian cancer and peritoneal carcinomatosis. Gynecologic Oncology. 2018; 150: 23–30.
[103] Dumont F, Passot C, Raoul J, Kepenekian V, Lelièvre B, Boisdron-Celle M, et al. A phase i dose-escalation study of oxaliplatin delivered via a laparoscopic approach using pressurised intraperitoneal aerosol chemotherapy for advanced peritoneal metastases of gastrointestinal tract cancers. European Journal of Cancer. 2020; 140: 37–44.
[104] Solass W, Kerb R, Mürdter T, Giger-Pabst U, Strumberg D, Tempfer C, et al. Intraperitoneal chemotherapy of peritoneal carcinomatosis using pressurized aerosol as an alternative to liquid solution: first evidence for efficacy. Annals of Surgical Oncology. 2014; 21: 553–559.
[105] Mimouni M, Richard C, Adenot P, Letheule M, Tarrade A, Sandra O, et al. Pressurized intraperitoneal aerosol chemotherapy (PIPAC): increased intraperitoneal pressure does not affect distribution patterns but leads to deeper penetration depth of doxorubicin in a sheep model. BMC Cancer. 2021; 21: 461.
[106] Tan HL, Kim G, Charles CJ, Li RR, Jang CJ, Shabbir A, et al. Safety, pharmacokinetics and tissue penetration of PIPAC paclitaxel in a swine model. European Journal of Surgical Oncology. 2021; 47: 1124–1131.
[107] Tempfer CB, Winnekendonk G, Solass W, Horvat R, Giger-Pabst U, Zieren J, et al. Pressurized intraperitoneal aerosol chemotherapy in women with recurrent ovarian cancer: a phase 2 study. Gynecologic Oncology. 2015; 137: 223–228.
[108] Dueckelmann AM, Fink D, Harter P, Heinzelmann V, Marth C, Mueller M, et al. The use of PIPAC (pressurized intraperitoneal aerosol chemotherapy) in gynecological oncology: a statement by the Arbeitsgemeinschaft Gynaekologische Onkologie (AGO) Kommission Ovar, AGO Study Group, North-Eastern German Society of Gynaecologic Oncology (NOGGO), AGO Austria and AGO Switzerland. Archives of Gynecology and Obstetrics. 2018; 297: 837–846.
[109] Bakrin N, Tempfer C, Scambia G, De Simone M, Gabriel B, Grischke E, et al. PIPAC-OV3: a multicenter, open-label, randomized, two-arm phase III trial of the effect on progression-free survival of cisplatin and doxorubicin as Pressurized Intra-Peritoneal Aerosol Chemotherapy (PIPAC) vs. chemotherapy alone in pa-tients with platinum-resistant recurrent epithelial ovarian, fallop-ian tube or primary peritoneal cancer. Pleura and Peritoneum. 2018; 3: 20180114.
[110] Somashekhar SP, Ashwin KR, Rauthan A, Rohit KC. Pres-surized IntraPeritoneal Aerosol Chemotherapy vs. intravenous chemotherapy for unresectable peritoneal metastases secondary to platinum resistant ovarian cancer - study protocol for a randomized control trial. Pleura and Peritoneum. 2019; 4: 20180111.
[111] Alyami M, Mercier F, Siebert M, Bonnot P, Laplace N, Vil-leneuve L, et al. Unresectable peritoneal metastasis treated by pressurized intraperitoneal aerosol chemotherapy (PIPAC) lead-ing to cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. European Journal of Surgical Oncology. 2021; 47: 128–133.
[112] Pilati P, Mocellin S, Miotto D, Rossi CR, Codello L, Foletto M, et al. Stop-flow technique for locoregional delivery of antiblastic agents: literature review and personal experience. European Journal of Surgical Oncology. 2001; 28: 544–553.
[113] Meyer F, Ridwelski K, Gebauer T, Grote R, Martens-Lobenhoffer J, Lippert H. Pharmacokinetics of the antineoplastic drug mitomycin C in regional chemotherapy using the aortic stop flow technique in advanced pancreatic carcinoma. Chemotherapy. 2005; 51: 1–8.
[114] Averbach AM, Stuart OA, Sugarbaker TA, Stephens AD, Fernandez-Trigo V, Shamsa F, et al. Intraaortic stop-flow infusion: pharmacokinetic feasibility study of regional chemotherapy for unresectable gastrointestinal cancers. Annals of Surgical Oncology. 1995; 2: 325–331.
[115] Kuemmerle A, Decosterd LA, Buclin T, Liénard D, Stupp R, Chassot P, et al. A phase i pharmacokinetic study of hypoxic abdominal stop-flow perfusion with gemcitabine in patients with ad-vanced pancreatic cancer and refractory malignant ascites. Cancer Chemotherapy and Pharmacology. 2009; 63: 331–341.
[116] de Bree E, Romanos J, Tsogkas J, Askoxylakis J, Metaxari M, Michalakis J, et al. Complications and toxicity after abdominal and pelvic hypoxic stop-flow perfusion chemotherapy: incidence and assessment of risk factors. Annals of Surgical Oncology. 2012; 19: 3591–3597.
[117] Aigner KR, Gailhofer S, Aigner K. Hypoxic isolated abdominal perfusion breaks through chemoresistance in recurrent FIGO stage IIIC and IV ovarian cancer. Molecular and Clinical Oncol-ogy. 2021; 14: 129.
[118] Guadagni S, Clementi M, Masedu F, Fiorentini G, Sarti D, Deraco M, et al. A pilot study of the predictive potential of chemosen-sitivity and gene expression assays using circulating tumour cells from patients with recurrent ovarian cancer. International Journal of Molecular Sciences. 2020; 21: 4813.
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