Ultrasound-mediated blood-brain/blood-tumor barrier disruption improves outcomes with trastuzumab in a breast cancer brain metastasis model

Journal of Controlled Release

Volumn 163, Issue 3, 2012, Pages 277-284

  Park, Eun Joo ^a   Zhang, Yong Zhi ^a   Vykhodtseva, Natalia ^a   McDannold, Nathan ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Blood brain barrier; Breast cancer; Microbubbles; MRgFUS; Targeted drug delivery; Trastuzumab

Indexed keywords

BLOOD-BRAIN BARRIER; BREAST CANCER; MICROBUBBLES; MRGFUS; TARGETED DRUG DELIVERY; TRASTUZUMAB;

ANIMALS; BLOOD; BRAIN; DIAGNOSIS; DISEASES; DRUG DELIVERY; NONINVASIVE MEDICAL PROCEDURES; PATHOLOGY; RATS; SPEED CONTROL; TUMORS; ULTRASONIC APPLICATIONS; ULTRASONICS;

MONOCLONAL ANTIBODIES;

EPIDERMAL GROWTH FACTOR RECEPTOR 2; TRASTUZUMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD TUMOR BARRIER; BRAIN METASTASIS; BREAST CANCER; CANCER GROWTH; CANCER SURVIVAL; CONTROLLED STUDY; DRUG PENETRATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MALE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERMEABILITY BARRIER; PRIORITY JOURNAL; RAT; SURVIVAL TIME; ULTRASOUND THERAPY;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; HUMANS; MALE; MICROBUBBLES; RATS; RATS, NUDE; SONICATION;

EID: 84867359055     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.09.007     Document Type: Article

References (49)

1. T. Pienkowski, and C.C. Zielinski Trastuzumab treatment in patients with breast cancer and metastatic CNS disease Ann. Oncol. 21 2010 917 924
2. B. Leyland-Jones Human epidermal growth factor receptor 2-positive breast cancer and central nervous system metastases J. Clin. Oncol. 27 2009 5278 5286
3. Y. Tsukada, A. Fouad, J.W. Pickren, and W.W. Lane Central nervous system metastasis from breast carcinoma. Autopsy study Cancer 52 1983 2349 2354 (Pubitemid 14205961)
4. Z. Gabos, R. Sinha, J. Hanson, N. Chauhan, J. Hugh, J.R. Mackey, and B. Abdulkarim Prognostic significance of human epidermal growth factor receptor positivity for the development of brain metastasis after newly diagnosed breast cancer J. Clin. Oncol. 24 2006 5658 5663 (Pubitemid 46631306)
5. E.C. Kaal, and C.J. Vecht CNS complications of breast cancer: current and emerging treatment options CNS Drugs 21 2007 559 579 (Pubitemid 46984857)
6. S. Dawood, K. Broglio, F.J. Esteva, N.K. Ibrahim, S.W. Kau, R. Islam, K.D. Aldape, T.K. Yu, G.N. Hortobagyi, and A.M. Gonzalez-Angulo Defining prognosis for women with breast cancer and CNS metastases by HER2 status Ann. Oncol. 19 2008 1242 1248 (Pubitemid 351911952)
7. W.A. Hall, H.R. Djalilian, E.S. Nussbaum, and K.H. Cho Long-term survival with metastatic cancer to the brain Med. Oncol. 17 2000 279 286
8. M.E. Melisko, D.H. Moore, P.K. Sneed, F.J. De, and H.S. Rugo Brain metastases in breast cancer: clinical and pathologic characteristics associated with improvements in survival J. Neurooncol. 88 2008 359 365
9. A.S. Mahmoud-Ahmed, J.H. Suh, S.Y. Lee, R.L. Crownover, and G.H. Barnett Results of whole brain radiotherapy in patients with brain metastases from breast cancer: a retrospective study Int. J. Radiat. Oncol. Biol. Phys. 54 2002 810 817
10. E.L. Chang, and S. Lo Diagnosis and management of central nervous system metastases from breast cancer Oncologist 8 2003 398 410 (Pubitemid 37238868)
11. E. Alexander III, T.M. Moriarty, R.B. Davis, P.Y. Wen, H.A. Fine, P.M. Black, H.M. Kooy, and J.S. Loeffler Stereotactic radiosurgery for the definitive, noninvasive treatment of brain metastases J. Natl. Cancer Inst. 87 1995 34 40
12. P.M. Black, and M.D. Johnson Surgical resection for patients with solid brain metastases: current status J. Neurooncol. 69 2004 119 124 (Pubitemid 39256124)
13. D. Kondziolka, H. Kano, G.L. Harrison, H.C. Yang, D.N. Liew, A. Niranjan, A.M. Brufsky, J.C. Flickinger, and L.D. Lunsford Stereotactic radiosurgery as primary and salvage treatment for brain metastases from breast cancer. Clinical article J. Neurosurg. 114 2011 792 800
14. D.W. Andrews, C.B. Scott, P.W. Sperduto, A.E. Flanders, L.E. Gaspar, M.C. Schell, M. Werner-Wasik, W. Demas, J. Ryu, J.P. Bahary, L. Souhami, M. Rotman, M.P. Mehta, and W.J. Curran Jr. Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial Lancet 363 2004 1665 1672 (Pubitemid 38670323)
15. A.F. Eichler, E. Chung, D.P. Kodack, J.S. Loeffler, D. Fukumura, and R.K. Jain The biology of brain metastases-translation to new therapies Nat. Rev. Clin. Oncol. 8 2011 344 356
16. D. Fukumura, and R.K. Jain Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize J. Cell. Biochem. 101 2007 937 949 (Pubitemid 47040874)
17. P.R. Lockman, R.K. Mittapalli, K.S. Taskar, V. Rudraraju, B. Gril, K.A. Bohn, C.E. Adkins, A. Roberts, H.R. Thorsheim, J.A. Gaasch, S. Huang, D. Palmieri, P.S. Steeg, and Q.R. Smith Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer Clin. Cancer Res. 16 2010 5664 5678
18. A.M. Gonzalez-Angulo, B.T. Hennessy, K. Broglio, F. Meric-Bernstam, M. Cristofanilli, S.H. Giordano, T.A. Buchholz, A. Sahin, S.E. Singletary, A.U. Buzdar, and G.N. Hortobagyi Trends for inflammatory breast cancer: is survival improving? Oncologist 12 2007 904 912 (Pubitemid 47359132)
19. A.M. Brufsky, M. Mayer, H.S. Rugo, P.A. Kaufman, E. Tan-Chiu, D. Tripathy, I.C. Tudor, L.I. Wang, M.G. Brammer, M. Shing, M.U. Yood, and D.A. Yardley Central nervous system metastases in patients with HER2-positive metastatic breast cancer: incidence, treatment, and survival in patients from registHER Clin. Cancer Res. 17 2011 4834 4843
20. N.U. Lin, and E.P. Winer Brain metastases: the HER2 paradigm Clin. Cancer Res. 13 2007 1648 1655 (Pubitemid 46952930)
21. N.U. Lin, V. Dieras, D. Paul, D. Lossignol, C. Christodoulou, H.J. Stemmler, H. Roche, M.C. Liu, R. Greil, E. Ciruelos, S. Loibl, S. Gori, A. Wardley, D. Yardley, A. Brufsky, J.L. Blum, S.D. Rubin, B. Dharan, K. Steplewski, D. Zembryki, C. Oliva, D. Roychowdhury, P. Paoletti, and E.P. Winer Multicenter phase II study of lapatinib in patients with brain metastases from HER2-positive breast cancer Clin. Cancer Res. 15 2009 1452 1459
22. R.H. Bobo, D.W. Laske, A. Akbasak, P.F. Morrison, R.L. Dedrick, and E.H. Oldfield Convection-enhanced delivery of macromolecules in the brain Proc. Natl. Acad. Sci. U. S. A. 91 1994 2076 2080 (Pubitemid 24092045)
23. N.D. Doolittle, M.E. Miner, W.A. Hall, T. Siegal, E. Jerome, E. Osztie, L.D. McAllister, J.S. Bubalo, D.F. Kraemer, D. Fortin, R. Nixon, L.L. Muldoon, and E.A. Neuwelt Safety and efficacy of a multicenter study using intraarterial chemotherapy in conjunction with osmotic opening of the blood-brain barrier for the treatment of patients with malignant brain tumors Cancer 88 2000 637 647 (Pubitemid 30056941)
24. D.J. Guillaume, N.D. Doolittle, S. Gahramanov, N.A. Hedrick, J.B. Delashaw, and E.A. Neuwelt Intra-arterial chemotherapy with osmotic blood-brain barrier disruption for aggressive oligodendroglial tumors: results of a phase I study Neurosurgery 66 2010 48 58
25. W.M. Pardridge Drug and gene delivery to the brain: the vascular route Neuron 36 2002 555 558 (Pubitemid 35346750)
26. W.M. Pardridge Biopharmaceutical drug targeting to the brain J. Drug Target. 18 2010 157 167
27. K. Hynynen, N. McDannold, N. Vykhodtseva, and F.A. Jolesz Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits Radiology 220 2001 640 646 (Pubitemid 32799969)
28. N. Sheikov, N. McDannold, S. Sharma, and K. Hynynen Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium Ultrasound Med. Biol. 34 2008 1093 1104 (Pubitemid 351893156)
29. X. Shang, P. Wang, Y. Liu, Z. Zhang, and Y. Xue Mechanism of low-frequency ultrasound in opening blood-tumor barrier by tight junction J. Mol. Neurosci. 43 2011 364 369
30. N. Sheikov, N. McDannold, F. Jolesz, Y.Z. Zhang, K. Tam, and K. Hynynen Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood-brain barrier Ultrasound Med. Biol. 32 2006 1399 1409 (Pubitemid 44332656)
31. N. McDannold, N. Vykhodtseva, S. Raymond, F.A. Jolesz, and K. Hynynen MRI-guided targeted blood-brain barrier disruption with focused ultrasound: histological findings in rabbits Ultrasound Med. Biol. 31 2005 1527 1537 (Pubitemid 41606266)
32. K. Hynynen, N. McDannold, N. Vykhodtseva, S. Raymond, R. Weissleder, F.A. Jolesz, and N. Sheikov Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery J. Neurosurg. 105 2006 445 454 (Pubitemid 44358757)
33. B. Baseri, J.J. Choi, Y.S. Tung, and E.E. Konofagou Multi-modality safety assessment of blood-brain barrier opening using focused ultrasound and definity microbubbles: a short-term study Ultrasound Med. Biol. 36 2010 1445 1459
34. L.H. Treat, N. McDannold, N. Vykhodtseva, Y. Zhang, K. Tam, and K. Hynynen Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound Int. J. Cancer 121 2007 901 907 (Pubitemid 47106223)
35. J. Mei, Y. Cheng, Y. Song, Y. Yang, F. Wang, Y. Liu, and Z. Wang Experimental study on targeted methotrexate delivery to the rabbit brain via magnetic resonance imaging-guided focused ultrasound J. Ultrasound Med. 28 2009 871 880
36. M. Kinoshita, N. McDannold, F.A. Jolesz, and K. Hynynen Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption Proc. Natl. Acad. Sci. U. S. A. 103 2006 11719 11723 (Pubitemid 44182517)
37. F.Y. Yang, G.L. Lin, S.C. Horng, T.K. Chang, S.Y. Wu, T.T. Wong, and H.E. Wang Pulsed high-intensity focused ultrasound enhances the relative permeability of the blood-tumor barrier in a glioma-bearing rat model IEEE Trans. Ultrason. Ferroelectr. Freq. Control 58 2011 964 970
38. F.Y. Yang, M.C. Teng, M. Lu, H.F. Liang, Y.R. Lee, C.C. Yen, M.L. Liang, and T.T. Wong Treating glioblastoma multiforme with selective high-dose liposomal doxorubicin chemotherapy induced by repeated focused ultrasound Int. J. Nanomed. 7 2012 965 974
39. H.L. Liu, M.Y. Hua, P.Y. Chen, P.C. Chu, C.H. Pan, H.W. Yang, C.Y. Huang, J.J. Wang, T.C. Yen, and K.C. Wei Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment Radiology 255 2010 415 425
40. J.F. Jordao, C.A. yala-Grosso, K. Markham, Y. Huang, R. Chopra, J. McLaurin, K. Hynynen, and I. Aubert Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid-beta plaque load in the TgCRND8 mouse model of Alzheimer's disease PLoS One 5 e10549 2010
41. K. Hynynen, N. McDannold, N.A. Sheikov, F.A. Jolesz, and N. Vykhodtseva Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications NeuroImage 24 2005 12 20 (Pubitemid 39611021)
42. E. Martin, D. Jeanmonod, A. Morel, E. Zadicario, and B. Werner High-intensity focused ultrasound for noninvasive functional neurosurgery Ann. Neurol. 66 2009 858 861
43. N. McDannold, G.T. Clement, P. Black, F. Jolesz, and K. Hynynen Transcranial magnetic resonance imaging- guided focused ultrasound surgery of brain tumors: initial findings in 3 patients Neurosurgery 66 2010 323 332
44. M.C. Pilatou, E.A. Stewart, S.E. Maier, F.M. Fennessy, K. Hynynen, C.M. Tempany, and N. McDannold MRI-based thermal dosimetry and diffusion-weighted imaging of MRI-guided focused ultrasound thermal ablation of uterine fibroids J. Magn. Reson. Imaging 29 2009 404 411
45. Genentech Herceptin http://www.herceptin.com/metastatic/what-is/index.jsp (3-8-2012)
46. National Breast Cancer Coalition Trastuzumab (Herceptin®) http://www.knowbreastcancer.org/controversies/herceptin/ (3-8-2012)
47. U.S. Food and Drug Administration Trastuzumab, Genentech Herceptin approval letter http://www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/ HowDrugsareDevelopedandApproved/ApprovalApplications/ TherapeuticBiologicApplications/ucm091360.pdf (3-8-2012)
48. B. Wasita, H. Kamitani, Y. Kinoshita, M.H. Mamun, and T. Watanabe A rat glioblastoma model with diffuse leptomeningeal gliomatosis induced by intracarotid injection of C6 glioma cells Neurol. Res. 31 2009 453 462
49. W.M. Pardridge Blood-brain barrier delivery Drug Discov. Today 12 2007 54 61 (Pubitemid 46014479)