Combination therapy of radiofrequency ablation and bevacizumab monitored with power Doppler ultrasound in a murine model of hepatocellular carcinoma

International Journal of Hyperthermia

Volumn 28, Issue 8, 2012, Pages 766-775

  Thaker, Ashesh A ^a,b   Razjouyan, Faezeh ^a   Woods, David L ^a   Haemmerich, Dieter ^c   Sekhar, Kiran ^a,d   Wood, Bradford J ^a   Dreher, Matthew R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d ALBANY MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Bevacizumab; Hepatocellular carcinoma; Microvascular density; Power Doppler ultrasound; Radiofrequency ablation

Indexed keywords

BEVACIZUMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPPLER FLOWMETRY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MICROVASCULATURE; MOUSE; NONHUMAN; RADIOFREQUENCY ABLATION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CARCINOMA, HEPATOCELLULAR; CATHETER ABLATION; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MICE; MICE, NUDE; REGIONAL BLOOD FLOW; ULTRASONOGRAPHY, DOPPLER; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84869391989     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2012.724517     Document Type: Article

References (65)

1. Friedman M, Mikityansky I, Kam A, Libutti SK, Walther MM, Neeman Z, et al. Radiofrequency ablation of cancer. Cardiovasc Intervent Radiol 2004;27:427-434. (Pubitemid 39288080)
2. Gervais DA, McGovern FJ, Arellano RS, McDougal WS, Mueller PR. Radiofrequency ablation of renal cell carcinoma: Part 1, Indications, results, and role in patient management over a 6-year period and ablation of 100 tumors. Am J Roentgenol 2005;185:64-71.
3. Grenier N, Douws C, Perot V, Ferriere JM, Ravaud A. Combined radiofrequency ablation and antiangiogenic drug for the treatment of recurrent renal tumor. Urology 2009;73: e11-12.
4. Hines-Peralta A, Goldberg SN. Review of radiofrequency ablation for renal cell carcinoma. Clin Cancer Res 2004;10: S6328-6334.
5. Wood BJ, Ramkaransingh JR, Fojo T, Walther MM, Libutti SK. Percutaneous tumor ablation with radiofrequency. Cancer 2002;94:443-451. (Pubitemid 34081375)
6. Mulier S, Ni Y, Jamart J, Michel L, Marchal G, Ruers T. Radiofrequency ablation versus resection for resectable colorectal liver metastases: Time for a randomized trial? Ann Surg Oncol 2008;15:144-157.
7. Mulier S, Ni YC, Jamart J, Ruers T, Marchal G, Michel L. Local recurrence after hepatic radiofrequency coagulation YMultivariate meta-analysis and review of contributing factors. Ann Surg 2005;242:158-171. (Pubitemid 41033431)
8. Lu DS, Raman SS, Vodopich DJ, Wang M, Sayre J, Lassman C. Effect of vessel size on creation of hepatic radiofrequency lesions in pigs: Assessment of the 'heat sink' effect. Am J Roentgenol 2002;178:47-51. (Pubitemid 34016368)
9. Haemmerich D. Effects of micro- and macro-vascular perfusion during radiofrequency tumor ablation. Proc SPIE 2009;7181:R1-11.
10. Lu DS, Yu NC, Raman SS, Limanond P, Lassman C, Murray K, et al. Radiofrequency ablation of hepatocellular carcinoma: Treatment success as defined by histologic examination of the explanted liver. Radiology 2005;234:954-960. (Pubitemid 40250843)
11. Schutt DJ, Haemmerich D. Effects of variation in perfusion rates and of perfusion models in computational models of radio frequency tumor ablation. Med Phys 2008;35:3462-3470.
12. Mertyna P, Hines-Peralta A, Liu ZJ, Halpern E, Goldberg W, Goldberg SN. Radiofrequency ablation: Variability in heat sensitivity in tumors and tissues. J Vasc Interv Radiol 2007;18:647-654. (Pubitemid 46661177)
13. Mertyna P, Dewhirst MW, Halpern E, Goldberg W, Goldberg SN. Radiofrequency ablation: The effect of distance and baseline temperature on thermal dose required for coagulation. Int J Hyperthermia 2008;24:550-559.
14. Horkan C, Ahmed M, Liu Z, Gazelle GS, Solazzo SA, Kruskal JB, et al. Radiofrequency ablation: Effect of pharmacologic modulation of hepatic and renal blood flow on coagulation diameter in a VX2 tumor model. J Vasc Interv Radiol 2004;15:269-274. (Pubitemid 38316449)
15. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000;407:249-257.
16. Li WW. Tumor angiogenesis: Molecular pathology, therapeutic targeting, and imaging. Acad Radiol 2000;7:800-811.
17. Patan S, Munn LL, Jain RK. Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft: A novel mechanism of tumor angiogenesis. Microvasc Res 1996;51:260-272. (Pubitemid 26109370)
18. Kerbel RS. Tumor angiogenesis. N Engl J Med 2008;358:2039-2049. (Pubitemid 351656458)
19. Siemann DW, Chaplin DJ, Horsman MR. Vascular-targeting therapies for treatment of malignant disease. Cancer 2004;100:2491-2499. (Pubitemid 38715753)
20. Stevenson JP, Rosen M, Sun W, Gallagher M, Haller DG, Vaughn D, et al. Phase I trial of the antivascular agent combretastatin A4 phosphate on a 5-day schedule to patients with cancer: Magnetic resonance imaging evidence for altered tumor blood flow. J Clin Oncol 2003;21:4428-4438. (Pubitemid 46621821)
21. Zhao D, Chang CH, Kim JG, Liu H, Mason RP. In vivo nearinfrared spectroscopy and magnetic resonance imaging monitoring of tumor response to combretastatin A-4-phosphate correlated with therapeutic outcome. Int J Radiat Oncol Biol Phys 2011;80:574-581.
22. Thorpe PE. Vascular targeting agents as cancer therapeutics. Clin Cancer Res 2004;10:415-427. (Pubitemid 38173977)
23. Jenab-Wolcott J, Giantonio BJ. Bevacizumab: Current indications and future development for management of solid tumors. Expert Opin Biol Ther 2009;9:507-517.
24. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004;350:2335-2342. (Pubitemid 38702844)
25. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006;355:2542-2550. (Pubitemid 44917502)
26. Miller K, Wang M, Gralow J, Dickler M, Cobleigh M, Perez EA, et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med 2007;357:2666-2676.
27. Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004;10:145-147. (Pubitemid 38524883)
28. Huang G, Chen L. Tumor vasculature and microenvironment normalization: A possible mechanism of antiangiogenesis therapy. Cancer Biother Radiopharm 2008;23:661-667.
29. Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 2005;307:58-62. (Pubitemid 40093472)
30. Hakime A, Hines-Peralta A, Peddi H, Atkins MB, Sukhatme VP, Signoretti S, et al. Combination of radiofrequency ablation with antiangiogenic therapy for tumor ablation efficacy: Study in mice. Radiology 2007;244:464-470. (Pubitemid 47080878)
31. Sabir A, Schor-Bardach R, Wilcox CJ, Rahmanuddin S, Atkins MB, Kruskal JB, et al. Perfusion MDCT enables early detection of therapeutic response to antiangiogenic therapy. Am J Roentgenol 2008;191:133-139. (Pubitemid 351955217)
32. Hines-Peralta A, Sukhatme V, Regan M, Signoretti S, Liu ZJ, Goldberg SN. Improved tumor destruction with arsenic trioxide and radiofrequency ablation in three animal models. Radiology 2006;240:82-89. (Pubitemid 43902597)
33. Van der Veldt AA, Lubberink M, Bahce I, Walraven M, de Boer MP, Greuter HN, et al. Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: Implications for scheduling of anti-angiogenic drugs. Cancer Cell 2012;21:82-91.
34. Drevs J, Schneider V. The use of vascular biomarkers and imaging studies in the early clinical development of antitumour agents targeting angiogenesis. J Intern Med 2006;260:517-529. (Pubitemid 44772371)
35. Miller JC, Pien HH, Sahani D, Sorensen AG, Thrall JH. Imaging angiogenesis: Applications and potential for drug development. J Natl Cancer Inst 2005;97:172-187. (Pubitemid 40277367)
36. Padhani AR. MRI for assessing antivascular cancer treatments. Br J Radiol 2003;76:S60-80. (Pubitemid 39530317)
37. Schor-Bardach R, Alsop DC, Pedrosa I, Solazzo SA, Wang X, Marquis RP, et al. Does arterial spin-labeling MR imagingmeasured tumor perfusion correlate with renal cell cancer response to antiangiogenic therapy in a mouse model? Radiology 2009;251:731-742.
38. Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: Standardized quantities and symbols. J Magn Reson Imaging 1999;10:223-232. (Pubitemid 29463104)
39. Forsberg F, Ro RJ, Potoczek M, Liu JB, Merritt CR, James KM, et al. Assessment of angiogenesis: Implications for ultrasound imaging. Ultrasonics 2004;42:325-330.
40. Gee MS, Saunders HM, Lee JC, Sanzo JF, Jenkins WT, Evans SM, et al. Doppler ultrasound imaging detects changes in tumor perfusion during antivascular therapy associated with vascular anatomic alterations. Cancer Res 2001;61:2974-2982. (Pubitemid 32691943)
41. Jugold M, Palmowski M, Huppert J, Woenne EC, Mueller MM, Semmler W, et al. Volumetric high-frequency Doppler ultrasound enables the assessment of early antiangiogenic therapy effects on tumor xenografts in nude mice. Eur Radiol 2008;18:753-758.
42. Goertz DE, Yu JL, Kerbel RS, Burns PN, Foster FS. Highfrequency Doppler ultrasound monitors the effects of antivascular therapy on tumor blood flow. Cancer Res 2002;62:6371-6375. (Pubitemid 35364088)
43. Lavisse S, Lejeune P, Rouffiac V, Elie N, Bribes E, Demers B, et al. Early quantitative evaluation of a tumor vasculature disruptive agent AVE8062 using dynamic contrast-enhanced ultrasonography. Invest Radiol 2008;43:100-111.
44. Hardee ME, Eapen RJ, Rabbani ZN, Dreher MR, Marks J, Blackwell KL, et al. Her2/neu signaling blockade improves tumor oxygenation in a multifactorial fashion in Her2/neutumors. Cancer Chemother Pharmacol 2009;63:219-228.
45. Wang S, Shin IS, Hancock H, Jang BS, Kim HS, Lee SM, et al. Pulsed high intensity focused ultrasound increases penetration and therapeutic efficacy of monoclonal antibodies in murine xenograft tumors. J Control Realease 2012;162:218-224.
46. Tsushima Y, Funabasama S, Aoki J, Sanada S, Endo K. Quantitative perfusion map of malignant liver tumors, created from dynamic computed tomography data. Acad Radiol 2004;11:215-223. (Pubitemid 38140292)
47. Van Beers BE, Leconte I, Materne R, Smith AM, Jamart J, Horsmans Y. Hepatic perfusion parameters in chronic liver disease: Dynamic CT measurements correlated with disease severity. Am J Roentgenol 2001;176:667-673. (Pubitemid 32181963)
48. Breen MS, Breen M, Butts K, Chen L, Saidel GM, Wilson DL. MRI-guided thermal ablation therapy: Model and parameter estimates to predict cell death from MR thermometry images. Ann Biomed Eng 2007;35:1391-1403. (Pubitemid 47115173)
49. Solazzo S, Mertyna P, Peddi H, Ahmed M, Horkan C, Goldberg SN. RF ablation with adjuvant therapy: Comparison of external beam radiation and liposomal doxorubicin on ablation efficacy in an animal tumor model. Int J Hyperthermia 2008;24:560-567.
50. Haemmerich D, Chachati L, Wright AS, Mahvi DM, Lee Jr FT, Webster JG. Hepatic radiofrequency ablation with internally cooled probes: Effect of coolant temperature on lesion size. IEEE Trans Biomed Eng 2003;50:493-500. (Pubitemid 36438227)
51. Prakash P, Diederich CJ. Considerations for theoretical modelling of thermal ablation with catheter-based ultrasonic sources: Implications for treatment planning, monitoring and control. Int J Hyperthermia 2012;28:69-86.
52. Osaki T, Takagi S, Hoshino Y, Okumura M, Fujinaga T. Antitumor effects and blood flow dynamics after photodynamic therapy using benzoporphyrin derivative monoacid ring A in KLN205 and LM8 mouse tumor models. Cancer Lett 2007;248:47-57.
53. Le Serve AW, Hellmann K. Metastases and the normalization of tumour blood vessels by ICRF 159: A new type of drug action. Br Med J 1972;1:597-601.
54. Ansiaux R, Baudelet C, Jordan BF, Crokart N, Martinive P, DeWever J, et al. Mechanism of reoxygenation after antiangiogenic therapy using SU5416 and its importance for guiding combined antitumor therapy. Cancer Res 2006;66:9698-9704. (Pubitemid 44623670)
55. Dickson PV, Hamner JB, Sims TL, Fraga CH, Ng CY, Rajasekeran S, et al. Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy. Clin Cancer Res 2007;13:3942-3950. (Pubitemid 47037602)
56. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK. 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 2004;64:3731-3736. (Pubitemid 38697278)
57. Vlahovic G, Rabbani ZN, Herndon 2nd JE, Dewhirst MW, Vujaskovic Z. Treatment with imatinib in NSCLC is associated with decrease of phosphorylated PDGFR-beta and VEGF expression, decrease in interstitial fluid pressure and improvement of oxygenation. Br J Cancer 2006;95:1013-1019. (Pubitemid 44606827)
58. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004;6:553-563. (Pubitemid 40017699)
59. Roca C, Primo L, Valdembri D, Cividalli A, Declerck P, Carmeliet P, et al. Hyperthermia inhibits angiogenesis by a plasminogen activator inhibitor 1-dependent mechanism. Cancer Res 2003;63:1500-1507. (Pubitemid 36373635)
60. Goldberg SN, Kamel IR, Kruskal JB, Reynolds K, Monsky WL, Stuart KE, et al. Radiofrequency ablation of hepatic tumors: Increased tumor destruction with adjuvant liposomal doxorubicin therapy. Am J Roentgenol 2002;179:93-101. (Pubitemid 34694817)
61. Ahmed M, Liu Z, Lukyanov AN, Signoretti S, Horkan C, Monsky WL, et al. Combination radiofrequency ablation with intratumoral liposomal doxorubicin: Effect on drug accumulation and coagulation in multiple tissues and tumor types in animals. Radiology 2005;235:469-477. (Pubitemid 40571084)
62. Ahmed M, Monsky WE, Girnun G, Lukyanov A, D'Ippolito G, Kruskal JB, et al. Radiofrequency thermal ablation sharply increases intratumoral liposomal doxorubicin accumulation and tumor coagulation. Cancer Res 2003;63:6327-6333. (Pubitemid 37255180)
63. Monsky WL, Kruskal JB, Lukyanov AN, Girnun GD, Ahmed M, Gazelle GS, et al. Radio-frequency ablation increases intratumoral liposomal doxorubicin accumulation in a rat breast tumor model. Radiology 2002;224: 823-829. (Pubitemid 34919820)
64. Solazzo SA, Ahmed M, Schor-Bardach R, Yang W, Girnun GD, Rahmanuddin S, et al. Liposomal doxorubicin increases radiofrequency ablation-induced tumor destruction by increasing cellular oxidative and nitrative stress and accelerating apoptotic pathways. Radiology 2010;255: 62-74.
65. Wood BJ, Poon RT, Locklin JK, Dreher MR, Ng KK, Eugeni M, et al. Phase I study of heat-deployed liposomal doxorubicin during radiofrequency ablation for hepatic malignancies. J Vasc Interv Radiol 2012;23:248-255.