Intraperitoneal therapy for peritoneal tumors: Biophysics and clinical evidence

Nature Reviews Clinical Oncology

Volumn 7, Issue 2, 2010, Pages 108-115

  Ceelen, Wim P ^a   Flessner, Michael F ^b  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; CISPLATIN; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; FOLINIC ACID; MITOMYCIN C; MITOXANTRONE; OXALIPLATIN; PACLITAXEL;

APPENDIX TUMOR; AREA UNDER THE CURVE; BIOPHYSICS; BONE MARROW TOXICITY; CANCER RECURRENCE; CANCER SURVIVAL; CARCINOMATOUS PERITONITIS; CLINICAL PRACTICE; CLINICAL TRIAL; COLON CANCER; COLORECTAL CANCER; CYTOREDUCTIVE SURGERY; DOSE RESPONSE; DRUG ABSORPTION; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MEGADOSE; DRUG PENETRATION; DRUG TRANSPORT; HUMAN; HYPERTHERMIC THERAPY; NONHUMAN; OVARY CANCER; PATIENT SAFETY; PERITONEUM MESOTHELIOMA; PERITONEUM TUMOR; POSTOPERATIVE CARE; PRIORITY JOURNAL; REVIEW;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; COLORECTAL NEOPLASMS; COMBINED MODALITY THERAPY; FEMALE; HUMANS; INJECTIONS, INTRAPERITONEAL; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; TREATMENT OUTCOME;

EID: 76449101754     PISSN: 17594774     EISSN: 17594782     Source Type: Journal    
DOI: 10.1038/nrclinonc.2009.217     Document Type: Review

References (91)

1. Warrick, C. An improvement on the practice of tapping; whereby that operation, instead of a relief for symptoms, becomes an absolute cure for an ascites, exemplified in the case of Jane roman; and recommended to the consideration of the royal Society, by Christopher Warrick, of Truro, Surgeon. Philos. Trans. R. Soc. Lond. B. Biol. Sci 43, 12-19 (1744).
2. Weisberger, A. S., Levine, B. & Storaasli, J. P. Use of nitrogen mustard in treatment of serous effusions of neoplastic origin. J. Am. Med. Assoc. 159, 1704-1707 (1955).
3. Dedrick, r. L., Myers, C. E., Bungay, P. M. & Devita, v. T. Pharmacokinetic rationale for peritoneal drug administration in the treatment of ovarian cancer. Cancer Treat. Rep. 62, 1 (1978).
4. Markman, M. Strategies to examine new compounds for intraperitoneal use in ovarian cancer. Int. J. Gynecol. Cancer 18, 33-35 (2008).
5. Li, X. F. et al. visualization of hypoxia in microscopic tumors by immunofluorescent microscopy. Cancer Res. 67, 7646-7653 (2007).
6. Jakobsen, A. & Mortensen, L. S. On the importance of sensitivity to the dose-effect relationship in chemotherapy. Acta Oncol. 36, 375-381 (1997).
7. Alberts, D. S., Young, L., Mason, N. & Salmon, S. E. In vitro evaluation of anticancer drugs against ovarian cancer at concentrations achievable by intraperitoneal administration. Semin. Oncol. 12, 38-42 (1985).
8. Andrews, P. A., velury, S., Mann, S. C. & Howell, S. B. Cis-Diamminedichloroplatinum(Ii) accumulation in sensitive and resistant human ovarian carcinoma sells. Cancer Res. 48, 68-73 (1988).
9. Matsushima, Y. et al. Time-schedule dependency of the inhibiting activity of various anticancer drugs in the clonogenic assay. Cancer Chemother. Pharmacol. 14, 104-107 (1985).
10. Flessner, M., Henegar, J., Bigler, S. & Genous, L. Is the peritoneum a significant transport barrier in peritoneal dialysis? Perit. Dial. Int. 23, 542-549 (2003).
11. vazquez, v. D., Stuart, O. A., Mohamed, F. & Sugarbaker, P. Extent of parietal peritonectomy does not change intraperitoneal chemotherapy pharmacokinetics. Cancer Chemother. Rep. 52, 108-112 (2003).
12. Flessner, M. F. Endothelial glycocalyx and the peritoneal barrier. Perit. Dial. Int. 28, 6-12 (2008).
13. Howell, S. B. Pharmacologic principles of intraperitoneal chemotherapy for the treatment of ovarian cancer. Int. J. Gynecol. Cancer 18, 20-25 (2008).
14. Dedrick, r. L. Theoretical and experimental bases of intraperitoneal chemotherapy. Semin. Oncol. 12, 1-6 (1985).
15. Dedrick, r. L., Flessner, M. F., Collins, J. M. & Schultz, J. S. Is the peritoneum a membrane? Am. Soc. Artificial Intern. Organs J. 5, 1-5 (1982).
16. Flessner, M. F., Dedrick, r. L. & Schultz, J. S. A distributed model of peritoneal-plasma transport: theoretical consideratons. Am. J. Physiol. 246, r597-r607 (1984).
17. Heldin, C. H., rubin, K., Pietras, K. & Ostman, A. High interstitial fluid pressure-an obstacle in cancer therapy. Nat. Rev. Cancer 4, 806-813 (2004).
18. Flessner, M. F., Choi, J., Credit, K., Deverkadra, r. & Henderson, K. resistance of tumor interstitial pressure to the penetration of intraperitoneally delivered antibodies into metastatic ovarian tumors. Clin. Cancer Res. 11, 3117-3125 (2005).
19. Holzer, A. K. et al. The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol. Pharmacol. 66, 817-823 (2004).
20. Holzer, A. K., Katano, K., Clomp, L. W. J. & Howell, S. B. Cisplatin rapidly down-regulates its own influx transporter hCTr1 in cultured human ovarian carcinoma cells. Clin. Cancer Res. 10, 6744-6749 (2004). (Pubitemid 39346572)
21. Nederman, T. & Carlsson, J. Penetration and binding of vinblastine and 5-fluorouracil in cellular spheroids. Cancer Chemother. Pharmacol. 13, 131-135 (1984).
22. van de vaart, P. J. M. et al. Intraperitoneal cisplatin with regional hyperthermia in advanced ovarian cancer: Pharmacokinetics and cisplatin- DNA adduct formation in patients and ovarian cancer cell lines. Eur. J. Cancer 34, 148-154 (1998).
23. Minchinton, A. I. & Tannock, I. F. Drug penetration in solid tumors. Nat. Rev. Cancer 6, 583-592 (2006).
24. Primeau, A. J., rendon, A., Hedley, D., Lilge, L. & Tannock, I. F. The distribution of the anticancer drug doxorubicin in relation to blood vessels in solid tumors. Clin. Cancer Res. 11, 8782-8788 (2005).
25. Jang, S. H., Wientjes, M. G. & Au, J. L. S. Enhancement of paclitaxel delivery to solid tumors by apoptosis-inducing pretreatment: Effect of treatment schedule. J. Pharmacol. Exp. Ther. 296, 1035-1042 (2001).
26. Kondo, A. et al. Hypotonic intraperitoneal cisplatin chemotherapy for peritoneal carcinomatosis in mice. Br. J. Cancer 73, 1166-1170 (1996).
27. Esquis, P. et al. High intra-abdominal pressure enhances the penetration and antitumor effect of intraperitoneal cisplatin on experimental peritoneal carcinomatosis. Ann. Surg. 244, 106-112 (2006).
28. Jones, r. B. et al. High volume intraperitoneal chemotherapy with methotrexate in patients with cancer. Cancer Res. 41, 55-59 (1981).
29. Devita, v. T. Let's return to the "belly bath". Nat. Clin. Pract. Oncol. 3, 405 (2006).
30. Spratt, J. S., Adcock, r. A., Muskovin, M., Sherrill, W. & Mckeown, J. Clinical delivery system for intra-peritoneal hyperthermic chemotherapy. Cancer Res. 40, 256-260 (1980).
31. Issels, r. D. Hyperthermia adds to chemotherapy. Eur. J. Cancer 44, 2546-2554 (2008).
32. Sun, X. r. et al. Changes in tumor hypoxia induced by mild temperature hyperthermia as assessed by dual-tracer immunohistochemistry. Radiother. Oncol. 88, 269-276 (2008).
33. Los, G. et al. Optimization of intraperitoneal cisplatin therapy with regional hyperthermia in rats. Eur. J. Cancer 27, 472-477 (1991).
34. Los, G. et al. A rationale for carboplatin treatment and abdominal hyperthermia in cancers restricted to the peritoneal cavity. Cancer Res. 52, 1252-1258 (1992).
35. Pestieau, S. r., Belliveau, J. F., Griffin, H., Stuart, O. A. & Sugarbaker, P. H. Pharmacokinetics of intraperitoneal oxaliplatin: Experimental studies. J. Surg. Oncol. 76, 106-114 (2001).
36. Jacquet, P., Averbach, A., Stuart, O. A., Chang, D. & Sugarbaker, P. H. Hyperthermic intraperitoneal doxorubicin: pharmacokinetics, metabolism, and tissue distribution in a rat model. Cancer Chemother. Pharmacol. 41, 147-154 (1998).
37. Yan, T. D., Black, D., Savady, r. & Sugarbaker, P. H. Systematic review on the efficacy of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for peritoneal carcinomatosis from colorectal carcinoma. J. Clin. Oncol. 24, 4011-4019 (2006).
38. Markman, M. et al. responses to second-line cisplatin-based intraperitoneal therapy in ovarian cancer: influence of a prior response to intravenous cisplatin. J. Clin. Oncol. 9, 1801-1805 (1991).
39. Markman, M. et al. Evidence supporting the superiority of intraperitoneal cisplatin compared to intraperitoneal carboplatin for salvage therapy of small-volume residual ovarian cancer. Gynecol. Oncol. 50, 100-104 (1993).
40. Gadducci, A. & Conte, P. F. Intraperitoneal chemotherapy in the management of patients with advanced epithelial ovarian cancer: a critical review of the literature. Int. J. Gynecol. Cancer 18, 943-953 (2008).
41. Juretzka, M. M. et al. CA125 level as a predictor of progression-free survival and overall survival in ovarian cancer patients with surgically defined disease status prior to the initiation of intraperitoneal consolidation therapy. Gynecol. Oncol. 104, 176-180 (2007).
42. Francis, P. et al. Phase I feasibility and pharmacological study of weekly intraperitoneal paclitaxel: a Gynecologic Oncology Group pilot study. J. Clin. Oncol. 13, 2961-2967 (1995).
43. US National Insitutes of Health Intraperitoneal chemotherapy for ovarian cancer. http:// ctep.cancer.gov/highlights/docs/ clin-annc-010506.pdf (2009).
44. Kyrgiou, M., Salanti, G., Pavlidis, N., Paraskevaidis, E. & Ioannidis, J. P. A. Survival benefits with diverse chemotherapy regimens for ovarian cancer: Meta-analysis of multiple treatments. J. Natl Cancer Inst. 98, 1655-1663 (2006).
45. vergote, I. et al. Intraperitoneal chemotherapy in patients with advanced ovarian cancer: The con view. Oncologist 13, 410-414 (2008).
46. Ceelen, W. P. & Bracke, M. E. Peritoneal minimal residual disease in colorectal cancer: mechanisms, prevention, and treatment. Lancet Oncol. 10, 72-79 (2009).
47. Hribaschek, A. et al. Comparison of intraperitoneal with intravenous administration of taxol in experimental peritoneal carcinomatosis. Chemotherapy 53, 410-417 (2007).
48. vaillant, J. C. et al. Adjuvant intraperitoneal 5-fluorouracil in high-risk colon cancer: A multicenter phase III trial. Ann. Surg. 231, 449-456 (2000).
49. Nordlinger, B. et al. Adjuvant regional chemotherapy and systemic chemotherapy versus systemic chemotherapy alone in patients with stage II-III colorectal cancer: a multicentre randomised controlled phase III trial. Lancet Oncol. 6, 459-468 (2005).
50. Cotte, E. et al. Cytoreductive surgery and intraperitoneal chemohyperthermia for chemoresistant and recurrent advanced epithelial ovarian cancer: Prospective study of 81 patients. World J. Surg. 31, 1813-1821 (2007).
51. ryu, K. S. et al. Effects of intraperitoneal hyperthermic chemotherapy in ovarian cancer. Gynecol. Oncol. 94, 325-332 (2004).
52. Bijelic, L., Jonson, A. & Sugarbaker, P. H. Systematic review of cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy for treatment of peritoneal carcinomatosis in primary and recurrent ovarian cancer. Ann. Oncol. 18, 1943-1950 (2007).
53. Markman, M. Hyperthermic intraperitoneal chemotherapy in the management of ovarian cancer: a critical need for an evidence-based evaluation. Gynecol. Oncol. (in press) doi:10.1016/j.ygyno.2008.12.022.
54. Pai, r. K. & Longacre, T. A. Appendiceal mucinous tumors and pseudomyxoma peritonei: histologic features, diagnostic problems, and proposed classification. Adv. Anat. Pathol. 12, 291-311 (2005).
55. Smeenk, r. M., verwaal, v. J. & Zoetmulder, F. A. N. Pseudomyxoma peritonei. Cancer Treatment Rev. 33, 138-145 (2007).
56. Sugarbaker, P. H. & Chang, D. results of treatment of 385 patients with peritoneal surface spread of appendiceal malignancy. Ann. Surg. Oncol. 6, 727-731 (1999).
57. Elias, D. et al. Peritoneal pseudomyxoma: results of a systematic policy of complete cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Br. J. Surg. 95, 1164-1171 (2008).
58. Smeenk, r. M., verwaal, v. J., Antonini, N. & Zoetmulder, F. A. N. Survival analysis of pseudomyxoma peritonei patients treated by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Ann. Surg. 245, 104-109 (2007).
59. Sugarbaker, P. H. New standard of care for appendiceal epithelial neoplasms and pseudomyxoma peritonei syndrome? Lancet Oncol. 7, 69-76 (2006).
60. Miner, T. J. et al. Long-term survival following treatment of pseudomyxoma peritonei: an analysis of surgical therapy. Ann. Surg. 241, 300-308 (2005).
61. Jayne, D. G., Fook, S., Loi, C. & Seow-Choen, F. Peritoneal carcinomatosis from colorectal cancer. Br. J. Surg. 89, 1545-1550 (2002).
62. Glehen, O. et al. Cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for the management of peritoneal carcinomatosis from colorectal cancer: A multi-institutional study. J. Clin. Oncol. 22, 3284-3292 (2004).
63. verwaal, v. J., Bruin, S., Boot, H., van Slooten, G. & van Tinteren, H. 8-year follow-up of randomized trial: Cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy in patients with peritoneal carcinomatosis of colorectal cancer. Ann. Surg. Oncol. 15, 2426-2432 (2008).
64. verwaal, v. J. et al. randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer. J. Clin. Oncol. 21, 3737-3743 (2003).
65. Jacquet, P. & Sugarbaker, P. H. Current methodologies for clinical assessment of patients with peritoneal carcinomatosis. J. Exp. Clin. Cancer Res. 15, 49-58 (1996).
66. Swellengrebel, H. A. M., verwaal, v. J., Smeenk, r. M., Antonini, N. & Zoetmulder, F. A. N. Quantitative intra-operative assessment of peritoneal carcinomatosis-a comparison of three prognostic tools. 14th European Cancer Conference (ECCO 14) 3072 (Pergamon-Elsevier Science Ltd, Barcelona, Spain, 2007).
67. Kohne, C. H. et al. Clinical determinants of survival in patients with 5-fluorouracil-based treatment for metastatic colorectal cancer: results of a multivariate analysis of 3825 patients. Ann. Oncol. 13, 308-317 (2002).
68. Folprecht, G. et al. Effect of systemic chemotherapy (CTx) in patients with known peritoneal carcinomatosis (PC) from colorectal cancer [abstract 294]. ASCO Gastrointestinal Cancers Symposium (2007).
69. Elias, D. et al. Complete cytoreductive surgery plus intraperitoneal chemohyperthermia with oxaliplatin for peritoneal carcinomatosis of colorectal origin. J. Clin. Oncol. 27, 681-685 (2009).
70. Yan, T. D., Welch, L., Black, D. & Sugarbaker, P. H. 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). (Pubitemid 47054078)
71. Yan, T. D. et al. A systematic review and metaanalysis of the randomized controlled trials on adjuvant intraperitoneal chemotherapy for resectable gastric cancer. Ann. Surg. Oncol. 14, 2702-2713 (2007).
72. rao, G., Crispens, M. & rothenberg, M. L. Intraperitoneal chemotherapy for ovarian cancer: Overview and perspective. J. Clin. Oncol. 25, 2867-2872 (2007).
73. Chin, S. N. et al. Evaluation of an intraperitoneal chemotherapy program implemented at the Princess Margaret Hospital for patients with epithelial ovarian carcinoma. Gynecol. Oncol. 112, 450-454 (2009).
74. Smeenk, r. M., verwaal, v. J. & Zoetmulder, F. A. N. Toxicity and mortality of cytoreduction and intraoperative hyperthermic intraperitoneal chemotherapy in pseudomyxoma peritonei-a report of 103 procedures. Eur. J. Surg. Oncol. 32, 186-190 (2006).
75. verwaal, v. J., van Tinteren, H., ruth, S. v. & Zoetmulder, F. A. N. Toxicity of cytoreductive surgery and hyperthermic intra-peritoneal chemotherapy. J. Surg. Oncol. 85, 61-67 (2004).
76. Ceelen, W. P. et al. Safety and efficacy of hyperthermic intraperitoneal chemoperfusion with high-dose oxaliplatin in patients with peritoneal carcinomatosis. Ann. Surg. Oncol. 15, 535-541 (2008).
77. Shimizu, T., Maeta, M. & Koga, S. Influence of local hyperthermia on the Healing of small intestinal anastomoses in the rat. Br. J. Surg. 78, 57-59 (1991).
78. Pelz, J. O. W. et al. Hyperthermic intraperitoneal chemoperfusion (HIPEC) decrease wound strength of colonic anastomosis in a rat model. Intl J. Colorect. Dis. 22, 941-947 (2007).
79. Jacquet, P. et al. Analysis of morbidity and mortality in 60 patients with peritoneal carcinomatosis treated by cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy. Cancer 77, 2622-2629 (1996).
80. Alberts, D. S. et al. Intraperitoneal cisplatin plus intravenous cyclophosphamide versus intravenous cisplatin plus intravenous cyclophosphamide for stage III ovarian cancer. N. Engl. J. Med. 335, 1950-1955 (1996).
81. Markman, M. et al. 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 intergroup study of the Gynecologic Oncology Group, Southwestern Oncology Group, and Eastern Cooperative Oncology Group. J. Clin. Oncol. 19, 1001-1007 (2001).
82. Armstrong, D. K. et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N. Engl. J. Med. 354, 34-43 (2006).
83. Fujimoto, S. et al. Cytohistologic assessment of antitumor effects of intraperitoneal hyperthermic perfusion with mitomycin C for patients with gastric cancer with peritoneal metastasis. Cancer 70, 2754-2760 (1992).
84. van de vaart, P. J. M. et al. Intraperitoneal cisplatin with regional hyperthermia in advanced ovarian cancer: Pharmacokinetics and cisplatin- DNA adduct formation in patients and ovarian cancer cell lines. Eur. J. Cancer 34, 148-154 (1998).
85. Los, G. et al. A rationale for carboplatin treatment and abdominal hyperthermia in cancers restricted to the peritoneal cavity. Cancer Res. 52, 1252-1258 (1992).
86. Elias, D. et al. Heated intra-operative intraperitoneal oxaliplatin after complete resection of peritoneal carcinomatosis: pharmacokinetics and tissue distribution. Ann. Oncol. 13, 267-272 (2002). (Pubitemid 34704979)
87. Kuh, H. J., Jang, S. H., Wientjes, M. G., Weaver, J. r. & Au, J. L. S. Determinants of paclitaxel penetration and accumulation in human solid tumor. J. Pharmacol. Exp. Ther. 290, 871-880 (1999).
88. Morgan, r. J. et al. Phase I trial of intraperitoneal gemcitabine in the treatment of advanced malignancies primarily confined to the peritoneal cavity. Clin. Cancer Res. 13, 1232-1237 (2007).
89. Wiedemann, G., Mella, O., roszinski, S., Weiss, C. & Wagner, T. Hyperthermia enhances mitoxantrone cytotoxicity on human breast carcinoma and sarcoma xenografts in nude mice. Int. J. Radiat. Oncol. Biol. Phys. 24, 669-673 (1992).
90. Jacquet, P., Averbach, A., Stuart, O. A., Chang, D. & Sugarbaker, P. H. Hyperthermic intraperitoneal doxorubicin: pharmacokinetics, metabolism, and tissue distribution in a rat model. Cancer Chemother. Pharmacol. 41, 147-154 (1998).
91. Harada, S. et al. The antitumor effect of hyperthermia combined with fluorouracil and its analogues. Radiat. Res. 142, 232-241 (1995).