Rationale for Integrated Procedures: Cytoreduction and Hyperthermic Intraperitoneal Chemotherapy (HIPEC) Combined

  • Paolo Sammartino
  • Fabio Accarpio
  • Tommaso Cornali
  • Daniele Biacchi
  • Maurizio Cardi
  • Giammaria Fiorentini
Part of the Updates in Surgery book series (UPDATESSURG)

Abstract

Diffuse peritoneal malignancy raises major therapeutic problems and puts the patient’s life at high risk. In the past, systemic chemotherapy regimens functioned as a purely palliative approach, and palliative surgery aimed merely at reducing the symptoms, being unable to alter the natural course of the disease [1]. At the beginning of the 1990s, thanks to Sugarbaker’s pioneering efforts, research began to develop integrated procedures for treating peritoneal surface malignancies based on a therapeutic approach. This approach involved cytoreductive surgery (CRS) (peritonectomy procedures) combined with perioperative intraperitoneally administered chemotherapy (IP-CHT)—eventually integrated with hyperthermia—done immediately after surgical cytoreduction ended [hyperthermic intraperitoneal chemotherapy (HIPEC)], or during the early postoperative course [early postoperative intraperitoneal chemotherapy (EPIC)] [2]. The therapeutic rationale underlying integrated treatment originates from advances in systemic chemotherapy and improved knowledge about the pharmacological mechanisms underlying endoperitoneal drug delivery. The rationale for cancer chemotherapy hinges upon several well-known theoretical hypotheses. According to the Gompertzian cellular kinetic model (the tumor-growth profile can be depicted as an S-shaped curve), a tumor initially grows slowly and then rapidly becomes fast growing [3]. As the tumor enlarges, its blood supply and growth slows down, and a larger tumor cell percentage gradually enters a nonproliferative cell-cycle stage (Fig. 8.1).

Keywords

Peritoneal Carcinomatosis Interstitial Fluid Pressure Hyperthermic Intraperitoneal Chemotherapy Malignant Peritoneal Mesothelioma Early Postoperative Intraperitoneal Chemotherapy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Sadeghi B, Arvieux C, Glehen O et al (2000) Peritoneal carcinomatosis from non-gynecologic malignancies: results of the EVOCAPE 1 multicentric prospective study. Cancer 88:358–363PubMedGoogle Scholar
  2. 2.
    Sugarbaker P (1996) Peritoneal carcinomatosis: principle of management. Kluwer Academic PublisherGoogle Scholar
  3. 3.
    Norton L, Simon R, Brereton HD, Bogden AE (1976) Predicting the course of Gompertzian growth. Nature 264:542–545PubMedGoogle Scholar
  4. 4.
    Norton L, Simon R (1977) Tumor size, sensitivity to therapy, and design of treatment schedules. Cancer treatment reports 61:1307–1317PubMedGoogle Scholar
  5. 5.
    Norton L, Simon R (1986) The Norton-Simon hypothesis revisited. Cancer treatment reports 70:163–169PubMedGoogle Scholar
  6. 6.
    Goldie JH, Coldman AJ (1979) A mathematic model for relating the drug sensitivity of tumors to their spontaneous mutation rate. Cancer treatment reports 63:1727–1733PubMedGoogle Scholar
  7. 7.
    Norton L (1985) Implications of kinetic heterogeneity in clinical oncology. Seminars in oncology 12:231–249PubMedGoogle Scholar
  8. 8.
    Simpson-Herren L, Sanford AH, Holmquist JP (1976) Effects of surgery on the cell kinetics of residual tumor. Cancer treatment reports 60:1749–1760PubMedGoogle Scholar
  9. 9.
    Gunduz N, Fisher B, Saffer EA (1979) Effect of surgical removal on the growth and kinetics of residual tumor. Cancer research 39:3861–3865PubMedGoogle Scholar
  10. 10.
    Tanaka K, Inoue Y, Toiyama J (2010) The role of cytoreduction for metastatic and recurrent colorectal cancer in the era of multidisciplinary treatments J Clin Oncol 28:14091Google Scholar
  11. 11.
    Dedrick RL, Myers CE, Bungay PM, DeVita VT Jr (1978) Pharmacokinetic rationale for peritoneal drug administration in the treatment of ovarian cancer. Cancer treatment reports 62:1–11PubMedGoogle Scholar
  12. 12.
    Sugarbaker PH, Van der Speeten K, Anthony Stuart O, Chang D (2011) Impact of surgical and clinical factors on the pharmacology of intraperitoneal doxorubicin in 145 patients with peritoneal carcinomatosis. European journal of surgical oncology 37:719–726PubMedGoogle Scholar
  13. 13.
    Van der Speeten K, Stuart OA, Mahteme H, Sugarbaker PH (2009) A pharmacologic analysis of intraoperative intracavitary cancer chemotherapy with doxorubicin. Cancer chemotherapy and pharmacology 263:799–805Google Scholar
  14. 14.
    Rubin J, Clawson M, Planch A, Jones Q (1988) Measurements of peritoneal surface area in man and rat. The American journal of the medical sciences 295:453–458PubMedGoogle Scholar
  15. 15.
    Rossi CR, Deraco M, De Simone M et al (2004) Hyperthermic intraperitoneal intraoperative chemotherapy after cytoreductive surgery for the treatment of abdominal sarcomatosis: clinical outcome and prognostic factors in 60 consecutive patients. Cancer 100:1943–1950PubMedGoogle Scholar
  16. 16.
    Baratti D, Kusamura S, Martinetti A et al (2007) Prognostic value of circulating tumor markers in patients with pseudomyxoma peritonei treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Annals of surgical oncology 14:2300–2308PubMedGoogle Scholar
  17. 17.
    Glehen O, Schreiber V, Cotte E et al (2004) Cytoreductive surgery and intraperitoneal chemohyperthermia for peritoneal carcinomatosis arising from gastric cancer. Archives of surgery 139:20–26PubMedGoogle Scholar
  18. 18.
    Gardner SN (2000) A mechanistic, predictive model of dose-response curves for cell cycle phase-specific and -nonspecific drugs. Cancer research 60:1417–1425PubMedGoogle Scholar
  19. 19.
    Kusamura S, Elias D, Baratti D et al (2008) Drugs, carrier solutions and temperature in hyperthermic intraperitoneal chemotherapy. Journal of surgical oncology 98:247–252PubMedGoogle Scholar
  20. 20.
    Esquis P, Consolo D, Magnin G et al (2006) High intra-abdominal pressure enhances the penetration and antitumor effect of intraperitoneal cisplatin on experimental peritoneal carcinomatosis. Annals of surgery 244:106–112PubMedCentralPubMedGoogle Scholar
  21. 21.
    Gonzalez-Moreno S, Gonzalez-Bayon L, Ortega-Perez G (2012) Hyperthermic intraperitoneal chemotherapy: methodology and safety considerations. Surgical oncology clinics of North America 21:543–557PubMedGoogle Scholar
  22. 22.
    Ortega-Deballon P, Facy O, Jambet S et al (2010) Which method to deliver hyperthermic intraperitoneal chemotherapy with oxaliplatin? An experimental comparison of open and closed techniques. Annals of surgical oncology 17:1957–1963PubMedGoogle Scholar
  23. 23.
    Facy O, Al Samman S, Magnin G et al (2012) High pressure enhances the effect of hyperthermia in intraperitoneal chemotherapy with oxaliplatin: an experimental study. Annals of surgery 256:1084–1088PubMedGoogle Scholar
  24. 24.
    Katz MH, Barone RM (2003) The rationale of perioperative intraperitoneal chemotherapy in the treatment of peritoneal surface malignancies. Surgical oncology clinics of North America 12:673–688PubMedGoogle Scholar
  25. 25.
    Tannock IF, Lee CM, Tunggal JK et al (2002) Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy. Clinical cancer research 8:878–884PubMedGoogle Scholar
  26. 26.
    Los G, Mutsaers PH, Lenglet WJ et al (1990) Platinum distribution in intraperitoneal tumors after intraperitoneal cisplatin treatment. Cancer chemotherapy and pharmacology 25:389–394PubMedGoogle Scholar
  27. 27.
    Los G, Verdegaal EM, Mutsaers PH, McVie JG (1991) Penetration of carboplatin and cisplatin into rat peritoneal tumor nodules after intraperitoneal chemotherapy. Cancer chemotherapy and pharmacology 28:159–165PubMedGoogle Scholar
  28. 28.
    Dedrick RL, Flessner MF (1997) Pharmacokinetic problems in peritoneal drug administration: tissue penetration and surface exposure. Journal of the National Cancer Institute 89:480–487PubMedGoogle Scholar
  29. 29.
    Flessner MF, Choi J, Credit K et al (2005) Resistance of tumor interstitial pressure to the penetration of intraperitoneally delivered antibodies into metastatic ovarian tumors. Clinical cancer research 11:3117–3125PubMedGoogle Scholar
  30. 30.
    Grantab RH, Tannock IF (2012) Penetration of anticancer drugs through tumour tissue as a function of cellular packing density and interstitial fluid pressure and its modification by bortezomib. BMC cancer 12:214PubMedCentralPubMedGoogle Scholar
  31. 31.
    Molucon-Chabrot C, Isambert N, Benoit L et al (2006) Feasibility of using intraperitoneal epinephrine and cisplatin in patients with advanced peritoneal carcinomatosis. Anti-cancer drugs 17:1211–1217PubMedGoogle Scholar
  32. 32.
    Sticca RP, Dach BW (2003) Rationale for hyperthermia with intraoperative intraperitoneal chemotherapy agents. Surgical oncology clinics of North America 12:689–701PubMedGoogle Scholar
  33. 33.
    Dahl O, Dalene R, Schem BC, Mella O (1999) Status of clinical hyperthermia. Acta oncologica (Stockholm, Sweden) 38:863–873Google Scholar
  34. 34.
    Kampinga HH (2006) Cell biological effects of hyperthermia alone or combined with radiation or drugs: a short introduction to newcomers in the field. International journal of hyperthermia 22:191–196PubMedGoogle Scholar
  35. 35.
    Leunig M, Goetz AE, Dellian M et al (1992) Interstitial fluid pressure in solid tumors following hyperthermia: possible correlation with therapeutic response. Cancer research 52:487–490PubMedGoogle Scholar
  36. 36.
    Piche N, Leblond FA, Sideris L et al (2001) Rationale for heating oxaliplatin for the intraperitoneal treatment of peritoneal carcinomatosis: a study of the effect of heat on intraperitoneal oxaliplatin using a murine model. Annals of surgery 254:138–144Google Scholar
  37. 37.
    Souslova T, Averill-Bates DA (2004) Multidrug-resistant hela cells overexpressing MRP1 exhibit sensitivity to cell killing by hyperthermia: interactions with etoposide. International journal of radiation oncology, biology, physics 60:1538–1551PubMedGoogle Scholar
  38. 38.
    Elias D, Bonnay M, Puizillou JM et al (2002) Heated intra-operative intraperitoneal oxaliplatin after complete resection of peritoneal carcinomatosis: pharmacokinetics and tissue distribution. Annals of oncology 13:267–272PubMedGoogle Scholar
  39. 39.
    Mathe G, Kidani Y, Segiguchi M et al (1989) Oxalato-platinum or 1-OHP, a third-generation platinum complex: an experimental and clinical appraisal and preliminary comparison with cis-platinum and carboplatinum. Biomedicine & pharmacotherapy 43:237–250Google Scholar
  40. 40.
    de Gramont A, Tournigand C, Louvet C et al (1997) Oxaliplatin, folinic acid and 5-fluorouracil (FOLFOX) in pretreated patients with metastatic advanced cancer. The GERCOD. La Revue de medecine interne / fondee par la Societe nationale francaise de medecine interne 18:769–775PubMedGoogle Scholar
  41. 41.
    Van der Speeten K, Stuart OA, Mahteme H, Sugarbaker PH (2010) Pharmacology of perioperative 5-fluorouracil. Journal of surgical oncology 102:730–735PubMedGoogle Scholar
  42. 42.
    Elias D, Goere D, Dumont F et al (2014) Role of hyperthermic intraoperative peritoneal chemotherapy in the management of peritoneal metastases. European journal of cancer 50:332–340PubMedGoogle Scholar
  43. 43.
    Glockzin G, Rochon J, Arnold D et al (2013) A prospective multicenter phase II study evaluating multimodality treatment of patients with peritoneal carcinomatosis arising from appendiceal and colorectal cancer: the COMBATAC trial. BMC cancer 13:67PubMedCentralPubMedGoogle Scholar
  44. 44.
    Van der Speeten K, Stuart OA, Mahteme H, Sugarbaker PH (2011) Pharmacokinetic study of perioperative intravenous Ifosfamide. International journal of surgical oncology 2011:185092PubMedCentralPubMedGoogle Scholar
  45. 45.
    Fujiwara Y, Takiguchi S, Nakajima K et al (2012) Intraperitoneal docetaxel combined with S-1 for advanced gastric cancer with peritoneal dissemination. Journal of surgical oncology 105:38–42PubMedGoogle Scholar
  46. 46.
    Canbay E, Mizumoto A, Ichinose M et al (2014) Outcome data of patients with peritoneal carcinomatosis from gastric origin treated by a strategy of bidirectional chemotherapy prior to cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in a single specialized center in Japan. Annals of surgical oncology 21:1147–1152PubMedGoogle Scholar
  47. 47.
    Sugarbaker PH, Bijelic L (2012) Adjuvant bidirectional chemotherapy using an intraperitoneal port. Gastroenterology research and practice 2012:752643PubMedCentralPubMedGoogle Scholar
  48. 48.
    Verwaal VJ, van Ruth S, de Bree E et al (2003) Randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer. Journal of clinical oncology 21:3737–3743PubMedGoogle Scholar
  49. 49.
    Sugarbaker PH (2009) Epithelial appendiceal neoplasms. Cancer journal (Sudbury, Mass) 15:225–235Google Scholar
  50. 50.
    Weber T, Roitman M, Link KH (2012) Current status of cytoreductive surgery with hyperthermic intraperitoneal chemotherapy in patients with peritoneal carcinomatosis from colorectal cancer. Clinical colorectal cancer 11:167–176PubMedGoogle Scholar
  51. 51.
    Bachur NR, Gordon SL, Gee MV, Kon H (1979) NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proceedings of the National Academy of Sciences of the United States of America 76:954–957PubMedCentralPubMedGoogle Scholar
  52. 52.
    Barlogie B, Corry PM, Drewinko B (1980) In vitro thermochemotherapy of human colon cancer cells with cis-dichlorodiammineplatinum(II) and mitomycin C. Cancer research 40:1165–1168PubMedGoogle Scholar
  53. 53.
    Jacquet P, Averbach A, Stephens AD et al (1998) Heated intraoperative intraperitoneal mitomycin C and early postoperative intraperitoneal 5-fluorouracil: pharmacokinetic studies. Oncology 55:130–138PubMedGoogle Scholar
  54. 54.
    Van der Speeten K, Stuart OA, Chang D et al (2011) Changes induced by surgical and clinical factors in the pharmacology of intraperitoneal mitomycin C in 145 patients with peritoneal carcinomatosis. Cancer chemotherapy and pharmacology 68:147–156PubMedGoogle Scholar
  55. 55.
    van Ruth S, Verwaal VJ, Zoetmulder FA (2003) Pharmacokinetics of intraperitoneal mitomycin C. Surgical oncology clinics of North America 12:771–780PubMedGoogle Scholar
  56. 56.
    Esquivel J (2009) Technology of hyperthermic intraperitoneal chemotherapy in the United States, Europe, China, Japan, and Korea. Cancer journal (Sudbury, Mass) 15:249–254Google Scholar
  57. 57.
    Smeenk RM, Verwaal VJ, Zoetmulder FA (2006) Toxicity and mortality of cytoreduction and intraoperative hyperthermic intraperitoneal chemotherapy in pseudomyxoma peritonei—a report of 103 procedures. European journal of surgical oncology 32:186–190PubMedGoogle Scholar
  58. 58.
    Sugarbaker PH, Alderman R, Edwards G et al (2006) Prospective morbidity and mortality assessment of cytoreductive surgery plus perioperative intraperitoneal chemotherapy to treat peritoneal dissemination of appendiceal mucinous malignancy. Annals of surgical oncology 13:635–644PubMedGoogle Scholar
  59. 59.
    Cepeda V, Fuertes MA, Castilla J et al (2007) Biochemical mechanisms of cisplatin cytotoxicity. Anti-cancer agents in medicinal chemistry 7:3–18PubMedGoogle Scholar
  60. 60.
    Alberts DS, Liu PY, Hannigan EV et al (1996) Intraperitoneal cisplatin plus intravenous cyclophosphamide versus intravenous cisplatin plus intravenous cyclophosphamide for stage III ovarian cancer. The New England journal of medicine 335:1950–1955PubMedGoogle Scholar
  61. 61.
    Markman M, Bundy BN, Alberts DS et al (2001) Phase III trial of standard-dose intravenous cisplatin plus paclitaxel versus moderately high-dose carboplatin followed by intravenous paclitaxel and intraperitoneal cisplatin in small-volume stage III ovarian carcinoma: an inter-group study of the Gynecologic Oncology Group, Southwestern Oncology Group, and Eastern Cooperative Oncology Group. Journal of clinical oncology 19:1001–1007PubMedGoogle Scholar
  62. 62.
    Armstrong DK, Bundy B, Wenzel L et al (2006) Intraperitoneal cisplatin and paclitaxel in ovarian cancer. The New England journal of medicine 354:34–43PubMedGoogle Scholar
  63. 63.
    Urano M, Kuroda M, Nishimura Y (1999) For the clinical application of thermochemotherapy given at mild temperatures. International journal of hyperthermia 15:79–107PubMedGoogle Scholar
  64. 64.
    Los G, Mutsaers PH, van der Vijgh WJ et al (1989) Direct diffusion of cis-diamminedichloroplatinum(II) in intraperitoneal rat tumors after intraperitoneal chemotherapy: a comparison with systemic chemotherapy. Cancer research 49:3380–3384PubMedGoogle Scholar
  65. 65.
    van de Vaart PJ, van der Vange N, Zoetmulder FA et al (1998) Intraperitoneal 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 34:148–154PubMedGoogle Scholar
  66. 66.
    Raymond E, Faivre S, Woynarowski JM, Chaney SG (1998) Oxaliplatin: mechanism of action and antineoplastic activity. Seminars in oncology 25:4–12PubMedGoogle Scholar
  67. 67.
    Di Francesco AM, Ruggiero A, Riccardi R (2002) Cellular and molecular aspects of drugs of the future: oxaliplatin. Cellular and molecular life sciences 59:1914–1927PubMedGoogle Scholar
  68. 68.
    Elias DM, Sideris L (2003) Pharmacokinetics of heated intraoperative intraperitoneal oxali-platin after complete resection of peritoneal carcinomatosis. Surgical oncology clinics of North America 12:755–769PubMedGoogle Scholar
  69. 69.
    Jerremalm E, Hedeland M, Wallin I et al (2004) Oxaliplatin degradation in the presence of chloride: identification and cytotoxicity of the monochloro monooxalato complex. Pharmaceutical research 21:891–894PubMedGoogle Scholar
  70. 70.
    De Somer F, Ceelen W, Delanghe J et al (2008) Severe hyponatremia, hyperglycemia, and hyperlactatemia are associated with intraoperative hyperthermic intraperitoneal chemoperfusion with oxaliplatin. Peritoneal dialysis international 28:61–66PubMedGoogle Scholar
  71. 71.
    Stewart JHt, Shen P, Russell G et al (2008) A phase I trial of oxaliplatin for intraperitoneal hyperthermic chemoperfusion for the treatment of peritoneal surface dissemination from colorectal and appendiceal cancers. Annals of surgical oncology 15:2137–2145PubMedCentralPubMedGoogle Scholar
  72. 72.
    Fagotti A, Costantini B, Petrillo M et al (2012) Cytoreductive surgery plus HIPEC in platinum-sensitive recurrent ovarian cancer patients: a case-control study on survival in patients with two year follow-up. Gynecologic oncology 127:502–505PubMedGoogle Scholar
  73. 73.
    Esselen KM, Rodriguez N, Growdon W (2012) Patterns of recurrence in advanced epithelial ovarian, fallopian tube and peritoneal cancers treated with intraperitoneal chemotherapy. Gynecologic oncology 127:51–54PubMedGoogle Scholar
  74. 74.
    Argenta PA, Sueblinvong T, Geller MA et al (2013) Hyperthermic intraperitoneal chemotherapy with carboplatin for optimally-cytoreduced, recurrent, platinum-sensitive ovarian carcinoma: a pilot study. Gynecologic oncology 129:81–85PubMedGoogle Scholar
  75. 75.
    Czejka M, Jager W, Schuller J, Teherani D (1991) [Pharmacokinetics of carboplatin after intraperitoneal administration]. Archiv der Pharmazie 324:183–184PubMedGoogle Scholar
  76. 76.
    Jandial DD, Messer K, Farshchi-Heydari S (2009) Tumor platinum concentration following intraperitoneal administration of cisplatin versus carboplatin in an ovarian cancer model. Gynecologic oncology 115:362–366PubMedCentralPubMedGoogle Scholar
  77. 77.
    Tritton TR (1991) Cell surface actions of adriamycin. Pharmacology & therapeutics 49:293–309Google Scholar
  78. 78.
    Lane P, Vichi P, Bain DL, Tritton TR (1987) Temperature dependence studies of adriamycin uptake and cytotoxicity. Cancer research 47:4038–4042PubMedGoogle Scholar
  79. 79.
    Jacquet P, Averbach A, Stuart OA et al (1998) Hyperthermic intraperitoneal doxorubicin: pharmacokinetics, metabolism, and tissue distribution in a rat model. Cancer chemotherapy and pharmacology 41:147–154PubMedGoogle Scholar
  80. 80.
    Pilati P, Mocellin S, Rossi CR et al (2003) Doxorubicin activity is enhanced by hyperthermia in a model of ex vivo vascular perfusion of human colon carcinoma. World journal of surgery 27:640–646PubMedGoogle Scholar
  81. 81.
    Harrison LE, Bryan M, Pliner L, Saunders T. Phase I trial of pegylated liposomal doxorubicin with hyperthermic intraperitoneal chemotherapy in patients undergoing cytoreduction for advanced intra-abdominal malignancy. Annals of surgical oncology. 2008;15(5):1407–13.PubMedGoogle Scholar
  82. 82.
    Pestieau SR, Stuart OA, Chang D et al (1998) Pharmacokinetics of intraperitoneal gemcitabine in a rat model. Tumori 84:706–711PubMedGoogle Scholar
  83. 83.
    Sabbatini P, Aghajanian C, Leitao M et al (2004) Intraperitoneal cisplatin with intraperitoneal gemcitabine in patients with epithelial ovarian cancer: results of a phase I/II Trial. Clinical cancer research 10:2962–2967PubMedGoogle Scholar
  84. 84.
    Morgan RJ, Jr, Synold TW, Xi B et al (2007) Phase I trial of intraperitoneal gemcitabine in the treatment of advanced malignancies primarily confined to the peritoneal cavity. Clinical cancer research 13:1232–1237PubMedGoogle Scholar
  85. 85.
    Gamblin TC, Egorin MJ, Zuhowski EG et al (2008) Intraperitoneal gemcitabine pharmacokinetics: a pilot and pharmacokinetic study in patients with advanced adenocarcinoma of the pancreas. Cancer chemotherapy and pharmacology 62:647–653PubMedGoogle Scholar
  86. 86.
    Sugarbaker PH, Stuart OA, Bijelic L (2011) Intraperitoneal gemcitabine chemotherapy treatment for patients with resected pancreatic cancer: rationale and report of early data. International journal of surgical oncology 2011:161862PubMedCentralPubMedGoogle Scholar
  87. 87.
    Tentes AA, Kyziridis D, Kakolyris S et al (2012) Preliminary results of hyperthermic intraperitoneal intraoperative chemotherapy as an adjuvant in resectable pancreatic cancer. Gastroenterology research and practice 2012:506571PubMedCentralPubMedGoogle Scholar
  88. 88.
    Sarosy G, Leyland-Jones B, Soochan P, Cheson BD (1988) The systemic administration of intravenous melphalan. Journal of clinical oncology 6:1768–1782PubMedGoogle Scholar
  89. 89.
    Urano M, Ling CC (2002) Thermal enhancement of melphalan and oxaliplatin cytotoxicity in vitro. International journal of hyperthermia 18:307–315PubMedGoogle Scholar
  90. 90.
    Testori A, Verhoef C, Kroon HM et al (2011) Treatment of melanoma metastases in a limb by isolated limb perfusion and isolated limb infusion. Journal of surgical oncology 104:397–404PubMedGoogle Scholar
  91. 91.
    Alberts DS, Chen HS, Chang SY, Peng YM (1980) The disposition of intraperitoneal bleomycin, melphalan, and vinblastine in cancer patients. Recent results in cancer 74:293–299Google Scholar
  92. 92.
    Glehen O, Stuart OA, Mohamed F, Sugarbaker PH (2004) Hyperthermia modifies pharmacokinetics and tissue distribution of intraperitoneal melphalan in a rat model. Cancer chemotherapy and pharmacology. 54:79–84PubMedGoogle Scholar
  93. 93.
    Sugarbaker PH, Stuart OA (2007) Pharmacokinetic and phase II study of heated intraoperative intraperitoneal melphalan. Cancer chemotherapy and pharmacology 59:151–155PubMedGoogle Scholar
  94. 94.
    Bijelic L, Sugarbaker PH, Stuart OA (2012) Hyperthermic intraperitoneal chemotherapy with melphalan: a summary of clinical and pharmacological data in 34 patients. Gastroenterology research and practice 2012:827534PubMedCentralPubMedGoogle Scholar
  95. 95.
    Ceelen WP, Pahlman L, Mahteme H (2007) Pharmacodynamic aspects of intraperitoneal cytotoxic therapy. Cancer treatment and research 134:195–214PubMedGoogle Scholar
  96. 96.
    Mohamed F, Sugarbaker PH (2003) Intraperitoneal taxanes. Surgical oncology clinics of North America 12:825–833PubMedGoogle Scholar
  97. 97.
    Rietbroek RC, Katschinski DM, Reijers MH et al (1997) Lack of thermal enhancement for taxanes in vitro. International journal of hyperthermia 13:525–533PubMedGoogle Scholar
  98. 98.
    Schrump DS, Zhai S, Nguyen DM et al (2002) Pharmacokinetics of paclitaxel administered by hyperthermic retrograde isolated lung perfusion techniques. The Journal of thoracic and cardiovascular surgery 123:686–694PubMedGoogle Scholar
  99. 99.
    Mohamed F, Stuart OA, Glehen O et al (2004) Docetaxel and hyperthermia: factors that modify thermal enhancement. Journal of surgical oncology 88:14–20PubMedGoogle Scholar
  100. 100.
    Bouquet W, Ceelen W, Adriaens E et al (2010) In vivo toxicity and bioavailability of Taxol and a paclitaxel/beta-cyclodextrin formulation in a rat model during HIPEC. Annals of surgical oncology 17:2510–2517PubMedGoogle Scholar
  101. 101.
    Guichard S, Chatelut E, Lochon I et al (1998) Comparison of the pharmacokinetics and efficacy of irinotecan after administration by the intravenous versus intraperitoneal route in mice. Cancer chemotherapy and pharmacology 42:165–170PubMedGoogle Scholar
  102. 102.
    Maruyama M, Toukairin Y, Baba H et al (2000) Experimental study on CPT-11 intraperitoneal chemotherapy—metabolism of CPT-11 in malignant ascites. Gan to kagaku ryoho Cancer & chemotherapy 27:1858–1860Google Scholar
  103. 103.
    Maruyama M, Toukairin Y, Baba H et al (2001) Pharmacokinetic study of the intraperitoneal administration of CPT-11 for patients with peritoneal seedings of gastric and colonic cancers. Gan to kagaku ryoho Cancer & chemotherapy 28:1505–1507Google Scholar
  104. 104.
    Elias D, Matsuhisa T, Sideris L et al (2004) Heated intra-operative intraperitoneal oxaliplatin plus irinotecan after complete resection of peritoneal carcinomatosis: pharmacokinetics, tissue distribution and tolerance. Annals of oncology 15:1558–1565PubMedGoogle Scholar
  105. 105.
    Gouy S, Uzan C, Pautier P et al (2013) Results of oxaliplatin-based hyperthermic intraperitoneal chemotherapy in recurrent ovarian granulosa cell tumors. European journal of obstetrics, gynecology, and reproductive biology 170:464–467PubMedGoogle Scholar
  106. 106.
    Pestieau SR, Stuart OA, Sugarbaker PH et al (2000) Multi-targeted antifolate (MTA): pharmacokinetics of intraperitoneal administration in a rat model. European journal of surgical oncology 26:696–700PubMedGoogle Scholar
  107. 107.
    Vogelzang NJ, Rusthoven JJ, Symanowski J et al (2003) Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. Journal of clinical oncology 21:2636–2644PubMedGoogle Scholar
  108. 108.
    Janne PA, Wozniak AJ, Belani CP et al (2005) Open-label study of pemetrexed alone or in combination with cisplatin for the treatment of patients with peritoneal mesothelioma: outcomes of an expanded access program. Clinical lung cancer 7:40–46PubMedGoogle Scholar
  109. 109.
    Chambers SK, Chow HH, Janicek MF et al (2012) Phase I trial of intraperitoneal pemetrexed, cisplatin, and paclitaxel in optimally debulked ovarian cancer. Clinical cancer research 18:2668–2678PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Italia 2015

Authors and Affiliations

  • Paolo Sammartino
    • 1
  • Fabio Accarpio
  • Tommaso Cornali
  • Daniele Biacchi
  • Maurizio Cardi
  • Giammaria Fiorentini
  1. 1.Department of Surgery “Pietro Valdoni”Sapienza University of RomeRomeItaly

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