Tumour tissue transport after intraperitoneal anticancer drug delivery

References

• Flessner MF. (2008). Endothelial glycocalyx and the peritoneal barrier. Perit Dial Int 28:6–12.
   PubMed Web of Science ®Google Scholar
• Gardner SN. (2000). A mechanistic, predictive model of dose-response curves for cell cycle phase-specific and -nonspecific drugs. Cancer Res 60:1417–25.
   PubMed Web of Science ®Google Scholar
• Markman M. (2008). Antineoplastic agents in the management of ovarian cancer: current status and emerging therapeutic strategies. Trends Pharmacol Sci 29:515–19.
   PubMed Web of Science ®Google Scholar
• El-Kareh AW, Secomb TW. (2004). A theoretical model for intraperitoneal delivery of cisplatin and the effect of hyperthermia on drug penetration distance. Neoplasia 6:117–27.
   PubMed Web of Science ®Google Scholar
• Baxter LT, Jain RK. (1989). Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. Microvasc Res 37:77–104.
   PubMed Web of Science ®Google Scholar
• Bird RB, Stewart WE, Lightfoot EN. (2007). Transport phenomena (revised 2nd ed.). New York: John Wiley & Sons.
   Google Scholar
• Messori L, Merlino A. (2016). Cisplatin binding to proteins: a structural perspective. Coord Chem Rev 315:67–89.
   Web of Science ®Google Scholar
• Ivanov AI, Christodoulou J, Parkinson JA, et al. (1998). Cisplatin binding sites on human albumin. J Biol Chem 273:14721–30.
   PubMed Web of Science ®Google Scholar
• Steuperaert M, Debbaut C, Segers P, Ceelen W. (in press). Modelling drug transport during intraperitoneal chemotherapy. Pleura and Peritoneum.
   Google Scholar
• Dedrick RL, Flessner MF. (1997). Pharmacokinetic problems in peritoneal drug administration: tissue penetration and surface exposure. J Natl Cancer Inst 89:480–7.
   PubMed Web of Science ®Google Scholar
• Los G, Mutsaers PH, Lenglet WJ, et al. (1990). Platinum distribution in intraperitoneal tumors after intraperitoneal cisplatin treatment. Cancer Chemother Pharmacol 25:389–94.
   PubMed Web of Science ®Google Scholar
• Heldin CH, Rubin K, Pietras K, Ostman A. (2004). High interstitial fluid pressure – an obstacle in cancer therapy. Nat Rev Cancer 4:806–13.
   PubMed Web of Science ®Google Scholar
• Young EW. (2013). Cells, tissues, and organs on chips: challenges and opportunities for the cancer tumor microenvironment. Integr Biol (Camb) 5:1096–109.
   PubMed Web of Science ®Google Scholar
• Li H, Fan X, Houghton J. (2007). Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem 101:805–15.
   PubMed Web of Science ®Google Scholar
• De Wever O, Mareel M. (2003). Role of tissue stroma in cancer cell invasion. J Pathol 200:429–47.
   PubMed Web of Science ®Google Scholar
• Jamin Y, Boult JK, Li J, et al. (2015). Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography. Cancer Res 75:1216–24.
   PubMed Web of Science ®Google Scholar
• Zaleska-Dorobisz U, Kaczorowski K, Pawlus A, et al. (2014). Ultrasound elastography – review of techniques and its clinical applications. Adv Clin Exp Med 23:645–55.
   PubMed Web of Science ®Google Scholar
• Baker AM, Bird D, Lang G, et al. (2013). Lysyl oxidase enzymatic function increases stiffness to drive colorectal cancer progression through FAK. Oncogene 32:1863–8.
   PubMed Web of Science ®Google Scholar
• Paszek MJ, Zahir N, Johnson KR, et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–54.
   PubMed Web of Science ®Google Scholar
• Sun Z, Guo SS, Fassler R. (2016). Integrin-mediated mechanotransduction. J Cell Biol 215:445–56.
   PubMed Web of Science ®Google Scholar
• Butcher DT, Alliston T, Weaver VM. (2009). A tense situation: forcing tumour progression. Nat Rev Cancer 9:108–22.
   PubMed Web of Science ®Google Scholar
• Chauhan VP, Lanning RM, Diop-Frimpong B, et al. (2009). Multiscale measurements distinguish cellular and interstitial hindrances to diffusion in vivo. Biophys J 97:330–6.
   PubMed Web of Science ®Google Scholar
• 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. Ann Surg 244:106–12.
   PubMed Web of Science ®Google Scholar
• Jacquet P, Stuart OA, Chang D, Sugarbaker PH. (1996). Effects of intra-abdominal pressure on pharmacokinetics and tissue distribution of doxorubicin after intraperitoneal administration. Anticancer Drugs 7:596–603.
   PubMed Web of Science ®Google Scholar
• 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. Ann Surg 256:1084–8.
   PubMed Web of Science ®Google Scholar
• Tempfer CB, Celik I, Solass W, et al. (2014). Activity of pressurized intraperitoneal aerosol chemotherapy (PIPAC) with cisplatin and doxorubicin in women with recurrent, platinum-resistant ovarian cancer: preliminary clinical experience. Gynecol Oncol 132:307–11.
   PubMed Web of Science ®Google Scholar
• Solass W, Kerb R, Murdter T, et al. (2014). Intraperitoneal chemotherapy of peritoneal carcinomatosis using pressurized aerosol as an alternative to liquid solution: first evidence for efficacy. Ann Surg Oncol 21:553–9.
   PubMed Web of Science ®Google Scholar
• Solass W, Giger-Pabst U, Zieren J, Reymond MA. (2013). Pressurized intraperitoneal aerosol chemotherapy (PIPAC): occupational health and safety aspects. Ann Surg Oncol 20:3504–11.
   PubMed Web of Science ®Google Scholar
• Blanco A, Giger-Pabst U, Solass W, et al. (2013). Renal and hepatic toxicities after pressurized intraperitoneal aerosol chemotherapy (PIPAC). Ann Surg Oncol 20:2311–16.
   PubMed Web of Science ®Google Scholar
• Venkatasubramanian R, Henson MA, Forbes NS. (2008). Integrating cell-cycle progression, drug penetration and energy metabolism to identify improved cancer therapeutic strategies. J Theor Biol 253:98–117.
   PubMed Web of Science ®Google Scholar
• Kyle AH, Huxham LA, Yeoman DM, Minchinton AI. (2007). Limited tissue penetration of taxanes: a mechanism for resistance in solid tumors. Clin Cancer Res 13:2804–10.
   PubMed Web of Science ®Google Scholar
• Toley BJ, Tropeano Lovatt ZG, Harrington JL, Forbes NS. (2013). Microfluidic technique to measure intratumoral transport and calculate drug efficacy shows that binding is essential for doxorubicin and release hampers Doxil. Integr Biol (Camb) 5:1184–96.
   PubMed Web of Science ®Google Scholar
• De Smet L, Ceelen W, Remon JP, Vervaet C. (2013). Optimization of drug delivery systems for intraperitoneal therapy to extend the residence time of the chemotherapeutic agent. ScientificWorldJournal 2013:720858.
   PubMedGoogle Scholar
• Van Oudheusden TR, Grull H, Dankers PY, De Hingh IH. (2015). Targeting the peritoneum with novel drug delivery systems in peritoneal carcinomatosis: a review of the literature. Anticancer Res 35:627–34.
   PubMed Web of Science ®Google Scholar
• Dakwar GR, Shariati M, Willaert W, et al. (2017). Nanomedicine-based intraperitoneal therapy for the treatment of peritoneal carcinomatosis – mission possible? Adv Drug Deliv Rev 108:13–24.
   PubMed Web of Science ®Google Scholar
• Sen A, Capitano ML, Spernyak JA, et al. (2011). Mild elevation of body temperature reduces tumor interstitial fluid pressure and hypoxia and enhances efficacy of radiotherapy in murine tumor models. Cancer Res 71:3872–80.
   PubMed Web of Science ®Google Scholar
• Hauck ML, Coffin DO, Dodge RK, et al. (1997). A local hyperthermia treatment which enhances antibody uptake in a glioma xenograft model does not affect tumour interstitial fluid pressure. Int J Hyperthermia 13:307–16.
   PubMed Web of Science ®Google Scholar
• Klaver YLB, Hendriks T, Lomme RMLM, et al. (2011). Hyperthermia and intraperitoneal chemotherapy for the treatment of peritoneal carcinomatosis: an experimental study. Ann Surg 254:125–30.
   PubMed Web of Science ®Google Scholar
• Los G, Sminia P, Wondergem J, et al. (1991). Optimisation of intraperitoneal cisplatin therapy with regional hyperthermia in rats. Eur J Cancer 27:472–7.
   PubMed Web of Science ®Google Scholar
• Zeamari S, Floot B, van der Vange N, Stewart FA. (2003). Pharmacokinetics and pharmacodynamics of cisplatin after intraoperative hyperthermic intraperitoneal chemoperfusion (HIPEC). Anticancer Res 23:1643–8.
   PubMed Web of Science ®Google Scholar
• Facy O, Radais F, Ladoire S, et al. (2011). Comparison of hyperthermia and adrenaline to enhance the intratumoral accumulation of cisplatin in a murine model of peritoneal carcinomatosis. J Exp Clin Cancer Res 30:4.
   PubMed Web of Science ®Google Scholar
• Moen I, Tronstad KJ, Kolmannskog O, et al. (2009). Hyperoxia increases the uptake of 5-fluorouracil in mammary tumors independently of changes in interstitial fluid pressure and tumor stroma. BMC Cancer 9:446.
   PubMed Web of Science ®Google Scholar
• Leunig M, Goetz AE, Gamarra F, et al. (1994). Photodynamic therapy-induced alterations in interstitial fluid pressure, volume and water content of an amelanotic melanoma in the hamster. Br J Cancer 69:101–3.
   PubMed Web of Science ®Google Scholar
• Perentes JY, Wang Y, Wang X, et al. (2014). Low-dose vascular photodynamic therapy decreases tumor interstitial fluid pressure, which promotes liposomal doxorubicin distribution in a murine sarcoma metastasis model. Transl Oncol 7:393–9.
   Web of Science ®Google Scholar
• Osborne EM, Briere TM, Hayes-Jordan A, et al. (2016). Survival and toxicity following sequential multimodality treatment including whole abdominopelvic radiotherapy for patients with desmoplastic small round cell tumor. Radiother Oncol 119:40–4.
   PubMed Web of Science ®Google Scholar
• Znati CA, Rosenstein M, Boucher Y, et al. (1996). Effect of radiation on interstitial fluid pressure and oxygenation in a human tumor xenograft. Cancer Res 56:964–8.
   PubMed Web of Science ®Google Scholar
• Davies Cde L, Lundstrom LM, Frengen J, et al. (2004). Radiation improves the distribution and uptake of liposomal doxorubicin (caelyx) in human osteosarcoma xenografts. Cancer Res 64:547–53.
   PubMed Web of Science ®Google Scholar
• Khosrawipour V, Bellendorf A, Khosrawipour C, et al. (2016). Irradiation does not increase the penetration depth of doxorubicin in normal tissue after pressurized intra-peritoneal aerosol chemotherapy (PIPAC) in an ex vivo model. In Vivo 30:593–7.
   PubMed Web of Science ®Google Scholar
• Sassaroli E, O’Neill BE. (2014). Modulation of the interstitial fluid pressure by high intensity focused ultrasound as a way to alter local fluid and solute movement: insights from a mathematical model. Phys Med Biol 59:6775–95.
   PubMed Web of Science ®Google Scholar
• O’Neill BE, Vo H, Angstadt M, et al. (2009). Pulsed high intensity focused ultrasound mediated nanoparticle delivery: mechanisms and efficacy in murine muscle. Ultrasound Med Biol 35:416–24.
   PubMed Web of Science ®Google Scholar
• Li T, Wang YN, Khokhlova TD, et al. (2015). Pulsed high-intensity focused ultrasound enhances delivery of doxorubicin in a preclinical model of pancreatic cancer. Cancer Res 75:3738–46.
   PubMed Web of Science ®Google Scholar
• Wang S, Shin IS, Hancock H, et al. (2012). Pulsed high intensity focused ultrasound increases penetration and therapeutic efficacy of monoclonal antibodies in murine xenograft tumors. J Control Release 162:218–24.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Jain RK. (2011). Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 10:417–27.
   PubMed Web of Science ®Google Scholar
• Fuso Nerini I, Cesca M, Bizzaro F, Giavazzi R. (2016). Combination therapy in cancer: effects of angiogenesis inhibitors on drug pharmacokinetics and pharmacodynamics. Chin J Cancer 35:61.
   PubMed Web of Science ®Google Scholar
• Gremonprez F, Descamps B, Izmer A, et al. (2015). Pretreatment with VEGF(R)-inhibitors reduces interstitial fluid pressure, increases intraperitoneal chemotherapy drug penetration, and impedes tumor growth in a mouse colorectal carcinomatosis model. Oncotarget 6:29889–900.
   PubMed Web of Science ®Google Scholar
• Skliarenko JV, Lunt SJ, Gordon ML, et al. (2006). Effects of the vascular disrupting agent ZD6126 on interstitial fluid pressure and cell survival in tumors. Cancer Res 66:2074–80.
   PubMed Web of Science ®Google Scholar
• Lindner P, Heath D, Howell S, et al. (1996). Vasopressin modulation of peritoneal, lymphatic, and plasma drug exposure following intraperitoneal administration. Clin Cancer Res 2:311–17.
   PubMed Web of Science ®Google Scholar
• Tsiftsis D, de Bree E, Romanos J, et al. (1999). Peritoneal expansion by artificially produced ascites during perfusion chemotherapy. Arch Surg 134:545–9.
   PubMedGoogle Scholar
• Mahteme H, Sundin A, Larsson B, et al. (2005). 5-FU uptake in peritoneal metastases after pretreatment with radioimmunotherapy or vasoconstriction: an autoradiographic study in the rat. Anticancer Res 25:917–22.
   PubMed Web of Science ®Google Scholar
• Duvillard C, Benoit L, Moretto P, et al. (1999). Epinephrine enhances penetration and anti-cancer activity of local cisplatin on rat sub-cutaneous and peritoneal tumors. Int J Cancer 81:779–84.
   PubMed Web of Science ®Google Scholar
• Guardiola E, Chauffert B, Delroeux D, et al. (2010). Intraoperative chemotherapy with cisplatin and epinephrine after cytoreductive surgery in patients with recurrent ovarian cancer: a phase I study. Anticancer Drugs 21:320–5.
   PubMed Web of Science ®Google Scholar
• Royer B, Kalbacher E, Onteniente S, et al. (2012). Intraperitoneal clearance as a potential biomarker of cisplatin after intraperitoneal perioperative chemotherapy: a population pharmacokinetic study. Br J Cancer 106:460–7.
   PubMed Web of Science ®Google Scholar
• Oman M, Lundqvist S, Gustavsson B, et al. (2005). Phase I/II trial of intraperitoneal 5-Fluorouracil with and without intravenous vasopressin in non-resectable pancreas cancer. Cancer Chemother Pharmacol 56:603–9.
   PubMed Web of Science ®Google Scholar
• Podobnik B, Sersa G, Miklavcic D. (2001). Effect of hydralazine on interstitial fluid pressure in experimental tumours and in normal tissue. In Vivo 15:417–24.
   PubMed Web of Science ®Google Scholar
• Olsson PO, Gustafsson R, In ’t Zandt R, et al. (2016). The tyrosine kinase inhibitor imatinib augments extracellular fluid exchange and reduces average collagen fibril diameter in experimental carcinoma. Mol Cancer Ther 15:2455–64.
   PubMed Web of Science ®Google Scholar
• Provenzano PP, Cuevas C, Chang AE, et al. (2012). Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21:418–29.
   PubMed Web of Science ®Google Scholar
• Hingorani SR, Harris WP, Beck JT, et al. (2016). Phase Ib study of PEGylated recombinant human hyaluronidase and gemcitabine in patients with advanced pancreatic cancer. Clin Cancer Res 22:2848–54.
   PubMed Web of Science ®Google Scholar
• Kato M, Hattori Y, Kubo M, Maitani Y. (2012). Collagenase-1 injection improved tumor distribution and gene expression of cationic lipoplex. Int J Pharm 423:428–34.
   PubMed Web of Science ®Google Scholar
• Eikenes L, Bruland OS, Brekken C, Davies Cde L. (2004). Collagenase increases the transcapillary pressure gradient and improves the uptake and distribution of monoclonal antibodies in human osteosarcoma xenografts. Cancer Res 64:4768–73.
   PubMed Web of Science ®Google Scholar
• Brown E, McKee T, diTomaso E, et al. (2003). Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 9:796–800.
   PubMed Web of Science ®Google Scholar
• Perentes JY, McKee TD, Ley CD, et al. (2009). In vivo imaging of extracellular matrix remodeling by tumor-associated fibroblasts. Nat Methods 6:143–5.
   PubMed Web of Science ®Google Scholar
• Chauhan VP, Martin JD, Liu H, et al. (2013). Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels. Nat Commun 4:2516.
   PubMed Web of Science ®Google Scholar
• Diop-Frimpong B, Chauhan VP, Krane S, et al. (2011). Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proc Natl Acad Sci U S A 108:2909–14.
   PubMed Web of Science ®Google Scholar
• Kumar V, Boucher Y, Liu H, et al. (2016). Noninvasive assessment of losartan-induced increase in functional microvasculature and drug delivery in pancreatic ductal adenocarcinoma. Transl Oncol 9:431–7.
   PubMed Web of Science ®Google Scholar
• Olive KP, Jacobetz MA, Davidson CJ, et al. (2009). Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324:1457–61.
   PubMed Web of Science ®Google Scholar
• Ko AH, LoConte N, Tempero MA, et al. (2016). A phase I study of FOLFIRINOX Plus IPI-926, a hedgehog pathway inhibitor, for advanced pancreatic adenocarcinoma. Pancreas 45:370–5.
   PubMed Web of Science ®Google Scholar
• Kim EJ, Sahai V, Abel EV, et al. (2014). Pilot clinical trial of hedgehog pathway inhibitor GDC-0449 (vismodegib) in combination with gemcitabine in patients with metastatic pancreatic adenocarcinoma. Clin Cancer Res 20:5937–45.
   Web of Science ®Google Scholar
• Sherman MH, Yu RT, Engle DD, et al. (2014). Vitamin D receptor-mediated stromal reprogramming suppresses pancreatitis and enhances pancreatic cancer therapy. Cell 159:80–93.
   PubMed Web of Science ®Google Scholar
• Shany S, Sigal-Batikoff I, Lamprecht S. (2016). Vitamin D and myofibroblasts in fibrosis and cancer: at cross-purposes with TGF-beta/SMAD signaling. Anticancer Res 36:6225–34.
   PubMed Web of Science ®Google Scholar
• Moschetta M, Pretto F, Berndt A, et al. (2012). Paclitaxel enhances therapeutic efficacy of the F8-IL2 immunocytokine to EDA-fibronectin-positive metastatic human melanoma xenografts. Cancer Res 72:1814–24.
   PubMed Web of Science ®Google Scholar
• Taghian AG, Abi-Raad R, Assaad SI, et al. (2005). Paclitaxel decreases the interstitial fluid pressure and improves oxygenation in breast cancers in patients treated with neoadjuvant chemotherapy: clinical implications. J Clin Oncol 23:1951–61.
   PubMed Web of Science ®Google Scholar
• Geretti E, Leonard SC, Dumont N, et al. (2015). Cyclophosphamide-mediated tumor priming for enhanced delivery and antitumor activity of her2-targeted liposomal doxorubicin (MM-302). Mol Cancer Ther 14:2060–71.
   PubMed Web of Science ®Google Scholar
• Hylander BL, Sen A, Beachy SH, et al. (2015). Tumor priming by Apo2L/TRAIL reduces interstitial fluid pressure and enhances efficacy of liposomal gemcitabine in a patient derived xenograft tumor model. J Control Release 217:160–9.
   PubMed Web of Science ®Google Scholar
• Lu Z, Tsai M, Lu D, et al. (2008). Tumor-penetrating microparticles for intraperitoneal therapy of ovarian cancer. J Pharmacol Exp Ther 327:673–82.
   PubMed Web of Science ®Google Scholar
• Sugahara KN, Teesalu T, Karmali PP, et al. (2010). Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328:1031–5.
   PubMed Web of Science ®Google Scholar
• Sugahara KN, Teesalu T, Karmali PP, et al. (2009). Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 16:510–20.
   PubMed Web of Science ®Google Scholar
• Akashi Y, Oda T, Ohara Y, et al. (2014). Anticancer effects of gemcitabine are enhanced by co-administered iRGD peptide in murine pancreatic cancer models that overexpressed neuropilin-1. Br J Cancer 110:1481–7.
   PubMed Web of Science ®Google Scholar
• Sugahara KN, Scodeller P, Braun GB, et al. (2015). A tumor-penetrating peptide enhances circulation-independent targeting of peritoneal carcinomatosis. J Control Release 212:59–69.
   PubMed Web of Science ®Google Scholar
• Simon-Gracia L, Hunt H, Scodeller P, et al. (2016). iRGD peptide conjugation potentiates intraperitoneal tumor delivery of paclitaxel with polymersomes. Biomaterials 104:247–57.
   PubMed Web of Science ®Google Scholar
• Patel KJ, Lee C, Tan Q, Tannock IF. (2013). Use of the proton pump inhibitor pantoprazole to modify the distribution and activity of doxorubicin: a potential strategy to improve the therapy of solid tumors. Clin Cancer Res 19:6766–76.
   PubMed Web of Science ®Google Scholar
• Yu M, Lee C, Wang M, Tannock IF. (2015). Influence of the proton pump inhibitor lansoprazole on distribution and activity of doxorubicin in solid tumors. Cancer Sci 106:1438–47.
   PubMed Web of Science ®Google Scholar