Influence of vascular normalization on interstitial flow and delivery of liposomes in tumors

Physics in Medicine and Biology

Volumn 60, Issue 4, 2015, Pages 1477-1496

  Ozturk, Deniz ^a   Yonucu, Sirin ^a   Yilmaz, Defne ^a   Unlu, Mehmet Burcin ^a  

^a BOGAZICI UNIVERSITY   (Turkey)

Author keywords

convective transport; drug delivery; drug extravasation; interstitial fluid pressure; tumor size

Indexed keywords

BLOOD; BLOOD VESSELS; CONTROLLED DRUG DELIVERY; DRUG DELIVERY; LIPOSOMES; TRANSPORT PROPERTIES; TUMORS;

BENEFICIAL EFFECTS; CONVECTIVE TRANSPORT; DRUG DISTRIBUTION; DRUG EXTRAVASATION; INTERSTITIAL FLUID PRESSURES; THERAPEUTIC AGENTS; TUMOR SIZE; VASCULAR NORMALIZATION;

TARGETED DRUG DELIVERY;

ANTINEOPLASTIC AGENT; LIPOSOME; NANOPARTICLE;

BIOLOGICAL MODEL; BLOOD PRESSURE; CAPILLARY PERMEABILITY; EXTRACELLULAR FLUID; HUMAN; METABOLISM; NEOPLASMS;

ANTINEOPLASTIC AGENTS; BLOOD PRESSURE; CAPILLARY PERMEABILITY; EXTRACELLULAR FLUID; HUMANS; LIPOSOMES; MODELS, BIOLOGICAL; NANOPARTICLES; NEOPLASMS;

EID: 84922295565     PISSN: 00319155     EISSN: 13616560     Source Type: Journal    
DOI: 10.1088/0031-9155/60/4/1477     Document Type: Article

References (67)

1. Batchelor T T et al 2007 AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients Cancer Cell 11 83-95
2. Boucher Y, Baxter L T and Jain R K 1990 Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy Cancer Res. 50 4478-84
3. Boucher Y and Jain R K 1992 Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse Cancer Res. 52 5110-4
4. Chauhan V P, Stylianopoulos T, Martin J D, Popović Z, Chen O, Kamoun W S, Bawendi M G, Fukumura D and Jain R K 2012 Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner Nat. Nanotechnol. 7 383-8
5. Curry F E 1984 Mechanics and thermodynamics of transcapillary exchange Handbook of Physiology ed E Renkin and C Michel (Bethesda, MD: American Physiological Society) pp 309-74
6. Dickson P V, Hagedorn N L, Hamner J B, Fraga C H, Ng C Y C, Stewart C F and Davidoff A M 2007a Interferon beta-mediated vessel stabilization improves delivery and efficacy of systemically administered topotecan in a murine neuroblastoma model J. Pediatr. Surg. 42 160-5
7. Dickson P V et al 2007b Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy Clin. Cancer Res. 13 3942-50
8. Dreher M R, Liu W, Michelich C R, Dewhirst M W, Yuan F and Chilkoti A 2006 Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers J. Natl Cancer Inst. 98 335-44
9. Folarin A A, Konerding M A, Timonen J, Nagl S and Pedley R B 2010 Three-dimensional analysis of tumour vascular corrosion casts using stereoimaging and micro-computed tomography Microvasc. Res. 80 89-98
10. Gabizon A, Catane R, Uziely B, Kaufman B, Safra T, Cohen R, Martin F, Huang A and Barenholz Y 1994 Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes Cancer Res. 54 987-92
11. Goel S, Duda D G, Xu L, Munn L L, Boucher Y, Fukumura D and Jain R K 2011 Normalization of the vasculature for treatment of cancer and other diseases Physiol. Rev. 91 1071-121
12. Goh Y M, Kong H L and Wang C H 2001 Simulation of the delivery of doxorubicin to hepatoma Pharm. Res. 18 761-70
13. Gray R, Bhattacharya S, Bowden C, Miller K and Comis R L 2009 Independent review of E2100: a phase III trial of bevacizumab plus paclitaxel versus paclitaxel in women with metastatic breast cancer J. Clin. Oncol. 27 4966-72
14. Grothey A and Galanis E 2009 Targeting angiogenesis: progress with anti-VEGF treatment with large molecules Nat. Rev. Clin. Oncol. 9 507-18
15. Hassid Y, Furman-Haran E, Margalit R, Eilam R and Degani H 2006 Noninvasive magnetic resonance imaging of transport and interstitial fluid pressure in ectopic human lung tumors Cancer Res. 66 4159-66
16. Hellmann K 2003 Dynamics of tumour angiogenesis: effect of razoxane-induced growth rate slowdown Clin. Exp. Metastasis 20 95-102
17. Hellmann K 2004 Recognition of tumor blood vessel normalization as a new antiangiogenic concept Nat. Med. 10 329-30
18. Hobbs S K, Monsky W L, Yuan F, Roberts W G, Griffith L, Torchilin V P and Jain R K 1998 Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment Proc. Natl Acad. Sci. USA 95 4607-12
19. Huang K et al 2012 Size-dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo ACS Nano 6 4483-93
20. Hubbard M E and Byrne H M 2012 Multiphase modelling of vascular tumour growth in two spatial dimensions J. Theor. Biol. 316 70-89
21. Hurwitz H et al 2004 Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer New Engl. J. Med. 350 2335-42
22. Jain R K 1987a Transport of molecules across tumor vasculature Cancer Metastasis Rev. 6 559-93
23. Jain R K 1987b Transport of molecules in the tumor interstitium: a review Cancer Res. 47 3039-51
24. Jain R K 1990 Physiological barriers to delivery of monoclonal antibodies and other macromolecules in tumors Cancer Res. 50 814s-9s
25. Jain R K 2005 Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy Science 307 58-62
26. Jain R K and Baxter L T 1988 Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure Cancer Res. 48 7022-32
27. Jain R K and Stylianopoulos T 2010 Delivering nanomedicine to solid tumors Nat. Rev.: Clin. Oncol. 7 653-64
28. Jain R K, Tong R T and Munn L L 2007 Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model Cancer Res. 67 2729-35
29. Laginha K M, Verwoert S, Charrois G J R and Allen T M 2005 Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors Clin. Cancer Res. 11 6944-9
30. Leu A J, Berk D A, Lymboussaki A, Alitalo K and Jain R K 2000 Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation Cancer Res. 60 4324-7
31. Liu J, Liao S, Diop-Frimpong B, Chen W, Goel S, Naxerova K, Ancukiewicz M, Boucher Y, Jain R K and Xu L 2012 TGF-β blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma Proc. Natl Acad. Sci. USA 109 16618-23
32. Liu J et al 2011 PDGF-D improves drug delivery and efficacy via vascular normalization, but promotes lymphatic metastasis by activating CXCR4 in breast cancer Clin. Cancer Res. 17 3638-48
33. Miles D W et al 2010 Phase III study of bevacizumab plus docetaxel compared with placebo plus docetaxel for the first-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer J. Clin. Oncol. 28 3239-47
34. Mufamadi M S, Pillay V, Choonara Y E, Du Toit L C, Modi G, Naidoo D and Ndesendo V M K 2011 A review on composite liposomal technologies for specialized drug delivery J. Drug Delivery 2011 939851
35. Netti P A, Baxter L T, Boucher Y, Skalak R and Rakesh K J 1997 Macro- and microscopic fluid transport in living tissues: application to solid tumors AIChE J. 43 818-34
36. Nugent L J and Jain R K 1984 Extravascular diffusion in normal and neoplastic tissues Cancer Res. 44 238-44
37. Owen M, Stamper I J, Muthana M, Richardson G W, Dobson J, Lewis C E and Byrne H M 2011 Mathematical modeling predicts synergistic antitumor effects of combining a macrophage-based, hypoxia-targeted gene therapy with chemotherapy Cancer Res. 71 2826-37
38. Panovska J, Byrne H M and Maini P K 2008 A theoretical study of the response of vascular tumours to different types of chemotherapy Math. Comput. Modelling 47 560-79
39. Perren T J et al 2011 A phase 3 trial of bevacizumab in ovarian cancer New Engl. J. Med. 365 2484-96
40. Phipps C and Kohandel M 2011 Mathematical model of the effect of interstitial fluid pressure on angiogenic behavior in solid tumors Comput. Math. Methods Med. 2011 843765
41. Plotkin S R, Stemmer-Rachamimov A O, Barker F G, Halpin C, Padera T P, Tyrrell A, Sorensen A G, Jain R K and di Tomaso E 2009 Hearing improvement after bevacizumab in patients with neurofibromatosis type 2 New Engl. J. Med. 361 358-67
42. Pluen A et al 2001 Role of tumor-host interactions in interstitial diffusion of macromolecules: cranial versus subcutaneous tumors Proc. Natl Acad. Sci. USA 98 4628-33
43. Pozrikidis C 2010 Numerical simulation of blood and interstitial flow through a solid tumor J. Math. Biol. 60 75-94
44. Reck M et al 2009 Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil J. Clin. Oncol. 27 1227-34
45. Reddy S T, Berk D A, Jain R K and Swartz M A 2006 A sensitive in vivo model for quantifying interstitial convective transport of injected macromolecules and nanoparticles J. Appl. Physiol. 101 1162-9
46. Robert N J et al 2011 RIBBON-1: randomized, double-blind, placebo-controlled, phase III trial of chemotherapy with or without bevacizumab for first-line treatment of human epidermal growth factor receptor 2-negative, locally recurrent or metastatic breast cancer J. Clin. Oncol. 29 1252-60
47. Saltz L B et al 2008 Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study J. Clin. Oncol. 26 2013-9
48. Sandler A, Gray R, Perry M C, Brahmer J, Schiller J H, Dowlati A, Lilenbaum R and Johnson D H 2006 Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer New Engl. J. Med. 355 2542-50
49. Sarin H 2010 Physiologic upper limits of pore size of different blood capillary types and another perspective on the dual pore theory of microvascular permeability J. Angiogenesis Res. 2 1540-9
50. Sarntinoranont M, Rooney F and Ferrari M 2003 Interstitial stress and fluid pressure within a growing tumor Ann. Biomed. Eng. 31 327-35
51. Segers J, Di Fazio V, Ansiaux R, Martinive P, Feron O, Wallemacq P and Gallez B 2006 Potentiation of cyclophosphamide chemotherapy using the anti-angiogenic drug thalidomide: importance of optimal scheduling to exploit the 'normalization' window of the tumor vasculature Cancer Lett. 244 129-35
52. Shieh A C and Swartz M A 2011 Regulation of tumor invasion by interstitial fluid flow Phys. Biol. 8 015012
53. Sinek J, Frieboes H, Zheng X and Cristini V 2004 Two-dimensional chemotherapy simulations demonstrate fundamental transport and tumor response limitations involving nanoparticles Biomed. Microdevices 6 297-309
54. Tebbutt N C et al 2010 Capecitabine, bevacizumab, and mitomycin in first-line treatment of metastatic colorectal cancer: results of the Australasian Gastrointestinal Trials Group Randomized Phase III MAX Study J. Clin. Oncol. 28 3191-8
55. Teicher B A, Dupuis N P, Robinson M F, Emi Y and Goff D A 1995 Antiangiogenic treatment (TNP-470/minocycline) increases tissue levels of anticancer drugs in mice bearing Lewis lung carcinoma Oncol. Res. 7 237-43
56. Tong R T, Boucher Y, Kozin S V, Winkler F, Hicklin D J and Jain R K 2004 Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors Cancer Res. 64 3731-6
57. Trédan O, Galmarini C M, Patel K and Tannock I F 2007 Drug resistance and the solid tumor microenvironment J. Natl Cancer Inst. 99 1441-54
58. van de Ven A L, Wu M, Lowengrub J, McDougall S R, Chaplain M a J, Cristini V, Ferrari M and Frieboes H B 2012 Integrated intravital microscopy and mathematical modeling to optimize nanotherapeutics delivery to tumors AIP Adv. 2 11208
59. Vleugel M M, Bos R, van der Groep P, Greijer A E, Shvarts A, Stel H V, van der Wall E and van Diest P J 2004 Lack of lymphangiogenesis during breast carcinogenesis J. Clin. Pathol. 57 746-51
60. Wildiers H, Guetens G, De Boeck G, Verbeken E, Landuyt B, Landuyt W, de Bruijn E A and van Oosterom A T 2003 Effect of antivascular endothelial growth factor treatment on the intratumoral uptake of CPT-11 Br. J. Cancer 88 1979-86
61. Willett C G et al 2004 Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer Nat. Med. 10 145-7
62. Wolmark N, Yothers G, O'Connell M J, Sharif S, Atkins J N, Seay T E, Feherenbacher L, O'Reilly S and Allegra C J 2009 A phase III trial comparing mFOLFOX6 to mFOLFOX6 plus bevacizumab in stage II or III carcinoma of the colon: results of NSABP Protocol C-08 45th Annual Meeting of the American Society of Clinical Oncology (Orlando, Florida, 29 May-2 June 2009) (Alexandria, VA: American Society of Clinical Oncology)
63. Wu J, Long Q, Xu S and Padhani A R 2009 Study of tumor blood perfusion and its variation due to vascular normalization by anti-angiogenic therapy based on 3D angiogenic microvasculature J. Biomech. 42 712-21
64. Wu M, Frieboes H B, McDougall S R, Chaplain M A J, Cristini V and Lowengrub J 2013 The effect of interstitial pressure on tumor growth: coupling with the blood and lymphatic vascular systems J. Theor. Biol. 320 131-51
65. Wu N Z, Da D, Rudoll T L, Needham D, Whorton A R and Dewhirst M W 1993 Increased microvascular permeability contributes to preferential accumulation of stealth liposomes in tumor tissue Cancer Res. 53 3765-70
66. Yuan F, Leunig M, Huang S K, Berk D A, Papahadjopoulos D and Jain R K 1994 Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft Cancer Res. 54 3352-6
67. Zhou Q and Gallo J M 2009 Differential effect of sunitinib on the distribution of temozolomide in an orthotopic glioma model Neuro-oncology 11 301-10