Comparison of photoacoustically derived hemoglobin and oxygenation measurements with contrast-enhanced ultrasound estimated vascularity and immunohistochemical staining in a breast cancer model

Ultrasonic Imaging

Volumn 37, Issue 1, 2015, Pages 42-52

  Eisenbrey, John R ^a   Merton, Daniel A ^a   Marshall, Andrew ^a,b   Liu, Ji Bin ^a   Fox, Traci B ^c   Sridharan, Anush ^a,d   Forsberg, Flemming ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b DREXEL UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d Drexel University   (United States)

Author keywords

angiogenesis; Cox 2; oxygenation; photoacoustics; ultrasound contrast agents

Indexed keywords

BLOOD; CELL ADHESION; DISEASES; ENDOTHELIAL CELLS; HEMOGLOBIN; MEDICAL IMAGING; PHOTOACOUSTIC EFFECT; PHYSIOLOGICAL MODELS; TUMORS; ULTRASONICS;

ANGIOGENESIS; CONTRAST ENHANCED ULTRASOUND; COX-2; IMMUNOHISTOCHEMICAL STAINING; MAXIMUM INTENSITY PROJECTION; PLATELET ENDOTHELIAL CELL ADHESION MOLECULES; ULTRASOUND CONTRAST AGENT; VASCULAR ENDOTHELIAL GROWTH FACTOR;

OXYGENATION;

CD31 ANTIGEN; CYCLOOXYGENASE 2; OXYGEN; VASCULOTROPIN A;

ANIMAL; BLOOD; COMPARATIVE STUDY; ECHOGRAPHY; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; HUMAN; IMAGE ENHANCEMENT; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE RAT; PHOTOACOUSTICS; VASCULARIZATION;

ANIMALS; ANTIGENS, CD31; CYCLOOXYGENASE 2; FEMALE; HUMANS; IMAGE ENHANCEMENT; IMMUNOHISTOCHEMISTRY; MAMMARY NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; OXYGEN; PHOTOACOUSTIC TECHNIQUES; RATS, NUDE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84913616194     PISSN: 01617346     EISSN: 10960910     Source Type: Journal    
DOI: 10.1177/0161734614527435     Document Type: Article

References (39)

1. Siegel R, Naishadham MA, Jemal A. Cancer statistics. CA Cancer J Clin. 2013 ; 63: 11-30
2. Guarneri V, Conte PF. The curability of breast cancer and the treatment of advanced disease. Eur J Nucl Med Mol Imaging. 2004 ; 31: S149-61
3. Therasse P, Arbuck SG, Eisenhauer EA, Wanders JA, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. J Natl Cancer Inst. 2000 ; 92: 205-16
4. Weidner N, Folkman J, Pozza F, Bevilacqua P, Allred EN, Moore DH, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast cancer. J Natl Cancer Inst. 1992 ; 84: 1875-87
5. Gasparini G, Harris AL. Clinical importance of the determination of tumor angiogenesis in breast carcinoma: much more than a new prognostic tool. J Clin Oncol. 1995 ; 13: 765-82
6. Eisenbrey JR, Forsberg F. Contrast-enhanced ultrasound for molecular imaging of angiogenesis. Eur J Nucl Med Mol Imaging. 2010 ; 37: S138-46
7. Goldberg BB, Raichlen JS, Forseberg F 2 nd ed.London: Martin Dunitz; 2001. London: Martin Dunitz ; 2001
8. Correas J, Bridal L, Lesavre A, Mejean A, Claudon M, Helenon O. Ultrasound contrast agents: properties, principles of action, tolerance and artifacts. Eur Radiol. 2001 ; 11: 1316-28
9. Lamuraglia M, Bridal SL, Santin M, Izzi G, Rixie O, Paradiso A, et al. Clinical relevance of contrast-enhanced ultrasound in monitoring anti-angiogenic therapy of cancer: current status and perspectives. Crt Rev Oncol Hematol. 2010 ; 73: 202-12
10. Lassau N, Koscielny S, Albiges L, Benatsou B, Chebil M, Roche A, et al. Metastatic renal cell carcinoma treated with sunitinib: early evaluation of treatment response using dynamic contrast enhanced ultrasonography. Clin Cancer Res. 2010 ; 16: 1216-25
11. Averkiou M, Lampaskis M, Kyriakopoulou K, Skarlos D, Klouvas G, Strouthos C, et al. Quantification of tumor microvascularity with respiratory gated contrast enhanced ultrasound for monitoring therapy. Ultrasound Med Biol. 2010 ; 36: 68-77
12. Lassau N, Lamuraglia M, Chami L, Leclere J, Bonvalot S, Terrier P, et al. Gastrointesitinal stromal tumors treated with imatinib: monitoring treatment response with contrast-enhanced sonography. AJR Am J Roentgenol. 2006 ; 187: 1267-73
13. Guibal A, Taillade L, Mulé S, Comperat E, Badachi Y, Golmard JL, et al. Noninvasive contrast-enhanced US quantitative assessment of tumor microcirculation in a murine model: effect of discontinuing anti-VEGF therapy. Radiology. 2010 ; 254: 420-9
14. Siri S, Flexman ML, Vlachos F, Huang J, Hernandez SL, Kim HK, et al. Contrast ultrasound imaging for identification of early responder tumor models to anti-angiogenic therapy. Ultrasound Med Biol. 2012 ; 38: 1019-29
15. Anderson CR, Rychak JJ, Backer M, Backer J, Ley K, Klibanov AL. scVEGF microbubble ultrasound contrast agents: a novel probe for ultrasound molecular imaging of tumor angiogenesis. Invest Radiol. 2010 ; 45: 579-85
16. Bachawal SV, Jensen KC, Lutz AM, Gambhir SS, Tranquart F, Tian L, et al. Earlier detection of breast cancer with ultrasound molecular imaging in a transgenic mouse model. Cancer Res. 2013 ; 73: 1689-98
17. Pochon S, Tardy I, Bussat P, Bettinger T, Brochot J, von Wronski M, et al. BR55: a lipopeptide-based VEGFR2-targeted ultrasound contrast agent for molecular imaging of angiogenesis. Invest Radiol. 2010 ; 45: 89-95
18. Bzyl J, Palmowski M, Rix A, Arns S, Hyvelin JM, Pochon S, et al. The high angiogenic activity in very early breast cancer enables reliable imaging with VEGFR2-targeted microbubbles (BR55). Eur Radiol. 2013 ; 23: 468-75
19. Forsberg F, Dicker AP, Thakur ML, Rawool NM, Liu JB, Shi WT, et al. Comparing contrast-enhanced ultrasound to immunohistochemical markers of angiogenesis in a human melanoma xenograft model: preliminary results. Ultrasound Med Biol. 2002 ; 28: 445-51
20. Du J, Li FH, Fang H, Xia JG, Zhu CX. Correlation of real-time gray scale contrast-enhanced ultrasonography with microvessel density and vascular endothelial growth factor expression for assessment of angiogenesis in breast lesions. J Ultrasound Med. 2008 ; 27: 821-31
21. Forsberg F, Ro RJ, Fox TB, Liu JB, Chiou SY, Potoczek M, et al. Contrast enhanced maximum intensity projection ultrasound imaging for assessing angiogenesis in murine glioma and breast tumor models: a comparative study. Ultrasonics. 2011 ; 51: 382-9
22. Eisenbrey JR, Wilson CC, Ro RJ, Fox TB, Liu JB, Chiou SY, et al. Correlation of ultrasound contrast agent derived blood flow parameters with immunohistochemical angiogenesis markers in murine xenograft tumor models. Ultrasonics. 2013 ; 53: 1384-91
23. Su JL, Wang B, Wilson KE, Bayer CL, Chen YS, Kim S, et al. Advances in clinical and biomedical applications of photoacoustic imaging. Expert Opin Med Diagn. 2010 ; 4: 497-510
24. Beard P. Biomedical photoacoustic imaging. Interface Focus. 2011 ; 1: 602-31
25. Laufer J, Elwell C, Delpy D, Beard P. In vitro measurement of absolute blood oxygen saturation using pulsed near-infrared photoacoustic spectroscopy: accuracy and resolution. Phys Med Biol. 2005 ; 50: 4409-28
26. Needles A, Heinmiller A, Sun J, Theodoropoulous C, Bates D, Hirson D, et al. Development and initial application of a fully integrated photoacoustic micro-ultrasound system. IEEE Trans Ultrason Ferroelectr Freq Control. 2013 ; 60: 888-97
27. Kitai T, Torii M, Sugie T, Kanao S, Mikami Y, Shiina T, et al. Photoacoustic mammography: initial clinical results. Breast Cancer. 2014 ; 21: 146-53
28. Lungu GF, Li ML, Xie X, Wang LV, Stoica G. In vivo imaging and characterization of hypoxia-induced neovascularization and tumor invasion. Int J Oncol. 2007 ; 30: 45-54
29. Laufer J, Johnson P, Zhang E, Treeby B, Cox B, Pedley B, et al. In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy. J Biomed Opt. 2012 ; 17: 056016
30. Hoyt K, Sorace A, Saini R. Quantitative mapping of tumor vascularity using volumetric contrast-enhanced ultrasound. Invest Radiol. 2012 ; 47: 167-74
31. Delorme S, Knopp MV. Non-invasive vascular imaging: assessing tumour vascularity. Eur Radiol. 1998 ; 8: 517-27
32. Zhou JH, Cao LH, Zheng W, Liu M, Fan F, Li AH. Contrast-enhanced gray-scale ultrasound for quantitative evaluation of tumor response to chemotherapy: preliminary results with a mouse hepatoma model. AJR Am J Roentgenol. 2011 ; 196: W13-7
33. Hlatky L, Hahnfeldt P, Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst. 2002 ; 94: 883-93
34. Batchelor TT, Sorensen AG, del Tomaso E, Zhang WT, Duda DG, Cohen KS, et al. AZD2171, a PAN-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell. 2007 ; 11: 83-95
35. Jain RK. Normalization for tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005 ; 307: 58-62
36. Zhuang H, Yang ZG, Chen HG, Peng YL, Li L. Time-intensity curve parameters in colorectal tumours measured using double-contrast-enhanced ultrasound: correlations with tumor angiogenesis. Colorectal Dis. 2012 ; 14: 181-7
37. Sethi G, Shanmugam MK, Ramachandran L, Kumar AP, Tergaonkar V. Multifaceted link between cancer and inflammation. Biosci Rep. 2012 ; 32: 1-15
38. Stratford IJ, Adams GE, Bremmer JC, Cole S, Edwards HS, Robertson N, et al. Manipulation and exploitation of the tumor environment for therapeutic benefit. Int J Radiat Biol. 1994 ; 65: 85-94
39. Perneger TV. What's wrong with Bonferroni adjustments. BMJ. 1998 ; 316: 1236-8