Efficient measurement of total tumor microvascularity ex vivo using a mathematical model to optimize volume subsampling

Journal of Biomedical Optics

Volumn 18, Issue 9, 2013, Pages

  Spring, Bryan Q ^a   Palanisami, Akilan ^a   Zheng, Lei Zak ^a   Blatt, Amy E ^c   Bryan Sears, R ^a,b   Hasan, Tayyaba ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b EMMANUEL COLLEGE   (United States)

^c HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

antiangiogenic therapy; antivascular therapy; cancer; fluorescence imaging; image analysis; immunohistochemistry; Microvessel density; photodynamic therapy

Indexed keywords

ANTI-ANGIOGENIC THERAPY; ANTIVASCULAR; CANCER; FLUORESCENCE IMAGING; IMMUNOHISTOCHEMISTRY; MICROVESSEL DENSITY;

BLOOD VESSELS; FLUORESCENCE; IMAGE ANALYSIS; IMAGE PROCESSING; MATHEMATICAL MODELS; NETWORK PROTOCOLS; PHOTODYNAMIC THERAPY; TUMORS;

DIAGNOSIS;

EID: 84887854723     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.JBO.18.9.096015     Document Type: Article

References (60)

1. J. Folkman, "Tumor angiogenesis: Therapeutic implications," N. Engl. J. Med. 285(21), 1182-1186 (1971).
2. M. A. Gimbrone, Jr. et al., "Tumor dormancy in vivo by prevention of neovascularization," J. Exp. Med. 136(2), 261-276 (1972).
3. H. Hurwitz et al., "Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer," N. Engl. J. Med. 350(23), 2335-2342 (2004). (Pubitemid 38702844)
4. B. Sennino and D. M. McDonald, "Controlling escape from angiogenesis inhibitors," Nat. Rev. Cancer 12(10), 699-709 (2012).
5. R. K. Jain, "Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy," Science 307(5706), 58-62 (2005). (Pubitemid 40093472)
6. V. P. Chauhan et al., "Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner," Nat. Nanotech. 7(6), 383-388 (2012).
7. T. Boehm et al., "Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance," Nature 390(6658), 404-407 (1997). (Pubitemid 28027321)
8. R. K. Jain et al., "Biomarkers of response and resistance to antiangiogenic therapy," Nat. Rev. Clin. Oncol. 6(6), 327-338 (2009).
9. B. J. Vakoc et al., "Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging," Nat. Med. 15(10), 1219-1223 (2009).
10. E. B. Brown et al., "In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy," Nat. Med. 7(7), 864-868 (2001). (Pubitemid 32691644)
11. T. Inai et al., "Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts," Am. J. Pathol. 165(1), 35-52 (2004). (Pubitemid 38821812)
12. R. P. J. Barretto et al., "Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy," Nat. Med. 17(2), 223-228 (2011).
13. M. E. Seaman, S. M. Peirce, and K. Kelly, "Rapid analysis of vessel elements (RAVE): A tool for studying physiologic, pathologic and tumor angiogenesis," PLoS One 6(6), e20807 (2011).
14. N. G. Horton et al., "In vivo three-photon microscopy of subcortical structures within an intact mouse brain," Nat. Photon 7(3), 205-209 (2013).
15. H. F. Zhang et al., "Functional photoacoustic microscopy for highresolution and noninvasive in vivo imaging," Nat. Biotechnol. 24(7), 848-851 (2006). (Pubitemid 44086627)
16. D. M. McDonald and P. L. Choyke, "Imaging of angiogenesis: from microscope to clinic," Nat. Med. 9(6), 713-725 (2003). (Pubitemid 36749220)
17. M.-A. Abdul-Karim et al., "Automated tracing and change analysis of angiogenic vasculature from in vivo multiphoton confocal image time series," Microvasc. Res. 66(2), 113-125 (2003). (Pubitemid 36962873)
18. J. A. Tyrrell et al., "Robust 3-D modeling of vasculature imagery using superellipsoids," IEEE Trans. Med. Imaging 26(2), 223-237 (2007). (Pubitemid 46362765)
19. Y. Gazit et al., "Fractal characteristics of tumor vascular architecture during tumor growth and regression," Microcirculation 4(4), 395-402 (1997). (Pubitemid 127675113)
20. B. J. Vakoc et al., "Cancer imaging by optical coherence tomography: Preclinical progress and clinical potential," Nat. Rev. Cancer 12(5), 363-368, (2012).
21. J. P. B. OConnor et al., "Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies," Nat. Rev. Clin. Oncol. 9(3), 167-177 (2012).
22. T. T. Batchelor et al., "AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients," Cancer Cell 11(1), 83-95 (2007). (Pubitemid 46075199)
23. T. Ragan et al., "High-resolution whole organ imaging using twophoton tissue cytometry," J. Biomed. Opt. 12(1), 014015 (2007).
24. T. Ragan et al., "Serial two-photon tomography for automated ex vivo mouse brain imaging," Nat. Methods 9(3), 255-258 (2012).
25. K. Chung et al., "Structural, and molecular interrogation of intact biological systems," Nature 497(7449), 332-337 (2013).
26. N. Weidner et al., "Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma," N. Engl. J. Med. 324(1), 1-8 (1991).
27. N. Weidner et al., "Tumor angiogenesis: A new significant and independent prognostic indicator in early-stage breast carcinoma," J. Natl. Cancer Inst. 84(24), 1875-1887 (1992). (Pubitemid 23004615)
28. P. B. Vermeulen et al., "Second International Consensus on the methodology and criteria of evaluation of angiogenesis quantification in solid human tumours," Eur. J. Cancer 38(12), 1564-1579 (2002). (Pubitemid 34876495)
29. L. Hlatky, P. Hahnfeldt, and J. Folkman, "Clinical application of antiangiogenic therapy: microvessel density, what it does and doesnt tell us," J. Natl. Cancer Inst. 94(12), 883-893 (2002). (Pubitemid 34778087)
30. J. A. Belien et al., "Fully automated microvessel counting and hot spot selection by image processing of whole tumour sections in invasive breast cancer," J. Clin. Pathol. 52(3), 184-192 (1999). (Pubitemid 29125410)
31. K. Wester et al., "Automatic quantification of microvessel density in urinary bladder carcinoma," Br. J. Cancer 81(8), 1363-1370 (1999).
32. K. S. Samkoe et al., "Imaging tumor variation in response to photodynamic therapy in pancreatic cancer xenograft models," Int. J. Radiat. Oncol. Biol. Phys. 76(1), 251-259 (2010).
33. C. G. Willett et al., "Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer," Nat. Med. 10(2), 145-147 (2004). (Pubitemid 38524883)
34. O. Gires et al., "Cytokeratin 8 associates with the external leaflet of plasma membranes in tumour cells," Biochem. Biophys. Res. Commun. 328(4), 1154-1162 (2005). (Pubitemid 40238755)
35. S. G. Mallat, "A theory for multiresolution signal decomposition: The wavelet representation," IEEE Trans. Pattern Anal. Mach. Intell. 11(7), 674-693 (1989).
36. P. Chu, E. Wu, and L. M. Weiss, "Cytokeratin 7 and cytokeratin 20 expression in epithelial neoplasms: A survey of 435 cases," Mod. Pathol. 13(9), 962-972 (2000).
37. S. Braun et al., "Cytokeratin-Positive Cells in the Bone Marrow and Survival of Patients with Stage I, II, or III Breast Cancer," N. Engl. J. Med. 342(8), 525-533 (2000). (Pubitemid 30117892)
38. G. M. van Dam et al., "Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor- targeting: first in-human results," Nat. Med. 17(10), 1315-1319 (2011).
39. S. Nagrath et al., "Isolation of rare circulating tumour cells in cancer patients by microchip technology," Nature 450(7173), 1235-1239 (2007).
40. F. M. Yakes et al., "Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth," Mol. Cancer Ther. 10(12), 2298-2308 (2011).
41. B. Sennino et al., "Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors," Cancer Discov. 2(3), 270-287 (2012).
42. B. Sennino et al., "Inhibition of c-Met reduces lymphatic metastasis in RIP-Tag2 transgenic mice," Cancer Res. 73(12), 3692-3703 (2013).
43. R. Kurzrock et al., "Activity of XL184 (Cabozantinib), an oral tyrosine kinase inhibitor, in patients with medullary thyroid cancer," J. Clin. Oncol. 29(19), 2660-2666 (2011).
44. A. N. Antoszyk et al., "Ranibizumab combined with verteporfin photodynamic therapy in neovascular age-related macular degeneration (focus): year 2 results," Am. J. Ophthalmol. 145(5), 862-874 (2008).
45. J. P. Celli et al., "Imaging and photodynamic therapy: mechanisms, monitoring, and optimization," Chem. Rev. 110(5), 2795-2838 (2010).
46. D. E. J. G. J. Dolmans, D. Fukumura, and R. K. Jain, "Timeline: Photodynamic therapy for cancer," Nat. Rev. Cancer 3(5), 380-387 (2003).
47. V. H. Fingar et al., "Analysis of acute vascular damage after photodynamic therapy using benzoporphyrin derivative (BPD)," Br. J. Cancer 79(11/12), 1702-1708 (1999). (Pubitemid 29132292)
48. K. Kurohane et al., "Photodynamic therapy targeted to tumor-induced angiogenic vessels," Cancer Lett. 167(1), 49-56 (2001). (Pubitemid 32373268)
49. B. Chen et al., "Combining vascular and cellular targeting regimens enhances the efficacy of photodynamic therapy," Int. J. Radiat. Oncol. Biol. Phys. 61(4), 1216-1226 (2005). (Pubitemid 40340918)
50. P. Carmeliet, "Angiogenesis in health and disease," Nat. Med. 9(6), 653-660 (2003). (Pubitemid 36749213)
51. J. Folkman, "Angiogenesis in cancer, vascular, rheumatoid and other disease," Nat. Med. 1(1), 27-30 (1995).
52. P.-H. Groop, C. Forsblom, and M. C. Thomas, "Mechanisms of Disease: Pathway-selective insulin resistance and microvascular complications of diabetes," Nat. Clin. Pract. Endocrinol. Metab. 1(2), 100-110 (2005).
53. A. Brown, L. R. Reynolds, and D. Bruemmer, "Intensive glycemic control and cardiovascular disease: An update," Nat. Rev. Cardiol. 7(7), 369-375 (2010).
54. R. N. Kalaria, "Neurodegenerative disease: Diabetes, microvascular pathology and Alzheimer disease," Nat. Rev. Neurol. 5(6), 305-306 (2009).
55. J. S. Miller et al., "Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues," Nat. Mater. 11(9), 768-774 (2012).
56. L. L. Y. Chiu et al., "Perfusable branching microvessel bed for vascularization of engineered tissues," Proc. Natl. Acad. Sci. 109(50), E3414-E3423 (2012).
57. "The quest for quantitative microscopy," Nat. Methods 9(7), 627 (2012).
58. J. R. Swedlow et al., "Informatics and quantitative analysis in biological imaging," Science 300(5616), 100-102 (2003). (Pubitemid 36423035)
59. H. Peng, "Bioimage informatics: A new area of engineering biology," Bioinformatics 24(17), 1827-1836 (2008).
60. B. L. Millard et al., "Adaptive informatics for multifactorial and highcontent biological data," Nat. Methods 8(6), 487-493 (2011).