Assessment of blood flow in hepatocellular carcinoma: Correlations of computed tomography perfusion imaging and circulating angiogenic factors

International Journal of Molecular Sciences

Volumn 14, Issue 9, 2013, Pages 17536-17552

  Chen, Ya Wen ^a,b   Pan, Huay Ben ^c,d,e   Tseng, Hui Hwa ^c,e   Hung, Yu Ting ^c   Huang, Jer Shyung ^c,e   Chou, Chen Pin ^c,e,f  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d I SHOU UNIVERSITY   (Taiwan)

^e NATIONAL YANG MING UNIVERSITY   (Taiwan)

^f FOOYIN UNIVERSITY   (Taiwan)

Author keywords

Blood flow; Circulating angiogenic factors; Ct perfusion; Hepatocellular carcinoma; Interleukin 8

Indexed keywords

ALPHA FETOPROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN;

ADULT; AGED; ARTERIAL FRACTION; ARTERY BLOOD FLOW; ARTICLE; BIOASSAY; CAPILLARY DENSITY; CLINICAL ARTICLE; COMPUTER ASSISTED TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY PERFUSION IMAGING; CONTROLLED STUDY; FEMALE; HEMODYNAMIC PARAMETERS; HISTOLOGY; HUMAN; HUMAN TISSUE; IMAGING SOFTWARE; IMMUNOHISTOCHEMISTRY; LIVER BLOOD FLOW; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER PARENCHYMA; MALE; MULTIDETECTOR COMPUTED TOMOGRAPHY; PORTAL VEIN BLOOD FLOW; PROTEIN BLOOD LEVEL; TOTAL BLOOD FLOW;

ADULT; ANGIOGENESIS INDUCING AGENTS; CARCINOMA, HEPATOCELLULAR; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MALE; MIDDLE AGED;

EID: 84883468366     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140917536     Document Type: Article

References (54)

1. Jemal, A.; Bray, F.; Center, M.M.; Ferlay, J.; Ward, E.; Forman, D. Global cancer statistics. CA Cancer J. Clin. 2011, 61, 69-90.
2. Yeh, C.N.; Lee, W.C.; Jeng, L.B.; Chen, M.F. Hepatic resection for hepatocellular carcinoma in TWN. Eur. J. Surg. Oncol. 2002, 28, 652-656.
3. Folkman, J. Tumor angiogenesis: Therapeutic implications. N. Engl. J. Med. 1971, 285, 1182-1186.
4. Asayama, Y.; Yoshimitsu, K.; Nishihara, Y.; Irie, H.; Aishima, S.; Taketomi, A.; Honda, H. Arterial blood supply of hepatocellular carcinoma and histologic grading: Radiologic-pathologic correlation. AJR Am. J. Roentgenol. 2008, 190, W28-W34.
5. Miles, K.A. Perfusion CT for the assessment of tumour vascularity: Which protocol? Br. J. Radiol. 2003, 76, S36-S42.
6. Cuenod, C.A.; Fournier, L.; Balvay, D.; Guinebretiere, J.M. Tumor angiogenesis: Pathophysiology and implications for contrast-enhanced MRI and CT assessment. Abdom. Imaging 2006, 31, 188-193.
7. Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86, 353-364.
8. Ellegala, D.B.; Leong-Poi, H.; Carpenter, J.E.; Klibanov, A.L.; Kaul, S.; Shaffrey, M.E.; Sklenar, J.; Lindner, J.R. Imaging tumor angiogenesis with contrast ultrasound and microbubbles targeted to alpha(v)beta3. Circulation 2003, 108, 336-341.
9. Yang, H.F.; Du, Y.; Ni, J.X.; Zhou, X.P.; Li, J.D.; Zhang, Q.; Xu, X.X.; Li, Y. Perfusion computed tomography evaluation of angiogenesis in liver cancer. Eur. Radiol. 2010, 20, 1424-1430.
10. Goh, V.; Halligan, S.; Daley, F.; Wellsted, D.M.; Guenther, T.; Bartram, C.I. Colorectal tumor vascularity: Quantitative assessment with multidetector CT-Do tumor perfusion measurements reflect angiogenesis? Radiology 2008, 249, 510-517.
11. Yi, C.A.; Lee, K.S.; Kim, E.A.; Han, J.; Kim, H.; Kwon, O.J.; Jeong, Y.J.; Kim, S. Solitary pulmonary nodules: Dynamic enhanced multi-detector row CT study and comparison with vascular endothelial growth factor and microvessel density. Radiology 2004, 233, 191-199.
12. Chen, Y.; Zhang, J.; Dai, J.; Feng, X.; Lu, H.; Zhou, C. Angiogenesis of renal cell carcinoma: Perfusion CT findings. Abdom. Imaging 2010, 35, 622-628.
13. Sahani, D.V.; Holalkere, N.S.; Mueller, P.R.; Zhu, A.X. Advanced hepatocellular carcinoma: CT perfusion of liver and tumor tissue-Initial experience. Radiology 2007, 243, 736-743.
14. Zhu, A.X.; Holalkere, N.S.; Muzikansky, A.; Horgan, K.; Sahani, D.V. Early antiangiogenic activity of bevacizumab evaluated by computed tomography perfusion scan in patients with advanced hepatocellular carcinoma. Oncologist 2008, 13, 120-125.
15. Pandharipande, P.V.; Krinsky, G.A.; Rusinek, H.; Lee, V.S. Perfusion imaging of the liver: Current challenges and future goals. Radiology 2005, 234, 661-673.
16. Sacco, R.; Faggioni, L.; Bargellini, I.; Ginanni, B.; Battaglia, V.; Romano, A.; Bertini, M.; Bresci, G.; Bartolozzi, C. Assessment of response to sorafenib in advanced hepatocellular carcinoma using perfusion computed tomography: Results of a pilot study. Dig. Liver Dis. 2013, doi:10.1016/j.dld.2013.03.004
17. Koh, T.S.; Thng, C.H.; Hartono, S.; Lee, P.S.; Choo, S.P.; Poon, D.Y.; Toh, H.C.; Bisdas, S. Dynamic contrast-enhanced CT imaging of hepatocellular carcinoma in cirrhosis: Feasibility of a prolonged dual-phase imaging protocol with tracer kinetics modeling. Eur. Radiol. 2009, 19, 1184-1196.
18. Ippolito, D.; Sironi, S.; Pozzi, M.; Antolini, L.; Ratti, L.; Alberzoni, C.; Leone, E.B.; Meloni, F.; Valsecchi, M.G.; Fazio, F. Hepatocellular carcinoma in cirrhotic liver disease: Functional computed tomography with perfusion imaging in the assessment of tumor vascularization. Acad. Radiol. 2008, 15, 919-927.
19. Chen, G.; Ma, D.Q.; He, W.; Zhang, B.F.; Zhao, L.Q. Computed tomography perfusion in evaluating the therapeutic effect of transarterial chemoembolization for hepatocellular carcinoma. World J. Gastroenterol. 2008, 14, 5738-5743.
20. Ippolito, D.; Sironi, S.; Pozzi, M.; Antolini, L.; Invernizzi, F.; Ratti, L.; Leone, E.B.; Fazio, F. Perfusion CT in cirrhotic patients with early stage hepatocellular carcinoma: Assessment of tumor-related vascularization. Eur. J. Radiol. 2008, 73, 148-152.
21. Ippolito, D.; Sironi, S.; Pozzi, M.; Antolini, L.; Ratti, L.; Meloni, F.; Invernizzi, F.; Valsecchi, M.G.; Fazio, F. Perfusion computed tomographic assessment of early hepatocellular carcinoma in cirrhotic liver disease: Initial observations. J. Comput. Assist. Tomogr. 2008, 32, 855-858.
22. Ippolito, D.; Bonaffini, P.A.; Ratti, L.; Antolini, L.; Corso, R.; Fazio, F.; Sironi, S. Hepatocellular carcinoma treated with transarterial chemoembolization: Dynamic perfusion-CT in the assessment of residual tumor. World J. Gastroenterol. 2010, 16, 5993-6000.
23. Ippolito, D.; Capraro, C.; Casiraghi, A.; Cestari, C.; Sironi, S. Quantitative assessment of tumour associated neovascularisation in patients with liver cirrhosis and hepatocellular carcinoma: Role of dynamic-CT perfusion imaging. Eur. Radiol. 2012, 22, 803-811.
24. Poon, R.T.; Fan, S.T.; Wong, J. Clinical implications of circulating angiogenic factors in cancer patients. J. Clin. Oncol. 2001, 19, 1207-1225.
25. Porta, C.; de Amici, M.; Quaglini, S.; Paglino, C.; Tagliani, F.; Boncimino, A.; Moratti, R.; Corazza, G.R. Circulating interleukin-6 as a tumor marker for hepatocellular carcinoma. Ann. Oncol. 2008, 19, 353-358.
26. Kim, S.J.; Choi, I.K.; Park, K.H.; Yoon, S.Y.; Oh, S.C.; Seo, J.H.; Choi, C.W.; Kim, B.S.; Shin, S.W.; Kim, Y.H.; et al. Serum vascular endothelial growth factor per platelet count in hepatocellular carcinoma: Correlations with clinical parameters and survival. Jpn. J. Clin. Oncol. 2004, 34, 184-190.
27. Ren, Y.; Poon, R.T.; Tsui, H.T.; Chen, W.H.; Li, Z.; Lau, C.; Yu, W.C.; Fan, S.T. Interleukin-8 serum levels in patients with hepatocellular carcinoma: Correlations with clinicopathological features and prognosis. Clin. Cancer Res. 2003, 9, 5996-6001.
28. Zhou, L.; Liu, J.; Luo, F. Serum tumor markers for detection of hepatocellular carcinoma. World J. Gastroenterol. 2006, 12, 1175-1181.
29. Fu, Q.; Zhu, J.; van Eyk, J.E. Comparison of multiplex immunoassay platforms. Clin. Chem. 2010, 56, 314-318.
30. Shan, Y.F.; Huang, Y.L.; Xie, Y.K.; Tan, Y.H.; Chen, B.C.; Zhou, M.T.; Shi, H.Q.; Yu, Z.P.; Song, Q.T.; Zhang, Q.Y. Angiogenesis and clinicopathologic characteristics in different hepatocellular carcinoma subtypes defined by EpCAM and alpha-fetoprotein expression status. Med. Oncol. 2011, 28, 1012-1016.
31. Petreaca, M.L.; Yao, M.; Liu, Y.; Defea, K.; Martins-Green, M. Transactivation of vascular endothelial growth factor receptor-2 by interleukin-8 (IL-8/CXCL8) is required for IL-8/CXCL8-induced endothelial permeability. Mol. Biol. Cell 2007, 18, 5014-5023.
32. Nilsson, M.B.; Langley, R.R.; Fidler, I.J. Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Res. 2005, 65, 10794-10800.
33. McClintock, J.Y.; Wagner, E.M. Role of IL-6 in systemic angiogenesis of the lung. J. Appl. Physiol. 2005, 99, 861-866.
34. Sugimachi, K.; Tanaka, S.; Terashi, T.; Taguchi, K.; Rikimaru, T. The mechanisms of angiogenesis in hepatocellular carcinoma: Angiogenic switch during tumor progression. Surgery 2002, 131, S135-S141.
35. Kim, K.R.; Moon, H.E.; Kim, K.W. Hypoxia-induced angiogenesis in human hepatocellular carcinoma. J. Mol. Med. 2002, 80, 703-714.
36. Heldin, C.H.; Westermark, B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 1999, 79, 1283-1316.
37. Luo, M.Y.; Shan, H.; Jiang, Z.B.; Li, L.F.; Huang, H.Q. Study on hepatocellular carcinoma-associated hepatic arteriovenous shunt using multidetector CT. World J. Gastroenterol. 2003, 9, 2455-2459.
38. Kornacker, M.; Roth, A.; Christensen, O.; Kratzschmar, J.; Wensing, G. Quantification of vascular endothelial growth factor, interleukin-8, and basic fibroblast growth factor in plasma of cancer patients and healthy volunteers-Comparison of ELISA and microsphere-based multiplexed immunoassay. Clin. Chem. Lab. Med. 2008, 46, 1256-1264.
39. Hsu, C.-Y.; Shen, Y.-C.; Yu, C.-W.; Hsu, C.; Hu, F.-C.; Hsu, C.-H.; Chen, B.-B.; Wei, S.-Y.; Cheng, A.-L.; Shih, T.T.-F. Dynamic contrast-enhanced magnetic resonance imaging biomarkers predict survival and response in hepatocellular carcinoma patients treated with sorafenib and metronomic tegafur/uracil. J. Hepatol. 2011, 55, 858-865.
40. Wang, J.; Chen, L.T.; Tsang, Y.M.; Liu, T.W.; Shih, T.T. Dynamic contrast-enhanced MRI analysis of perfusion changes in advanced hepatocellular carcinoma treated with an antiangiogenic agent: A preliminary study. AJR Am. J. Roentgenol. 2004, 183, 713-719.
41. Hafstrom, L.; Nobin, A.; Persson, B.; Sundqvist, K. Effects of catecholamines on cardiovascular response and blood flow distribution to normal tissue and liver tumors in rats. Cancer Res. 1980, 40, 481-485.
42. Bertolotto, M.; Pozzato, G.; Croce, L.S.; Nascimben, F.; Gasparini, C.; Cova, M.A.; Tiribelli, C. Blood flow changes in hepatocellular carcinoma after the administration of thalidomide assessed by reperfusion kinetics during microbubble infusion: Preliminary results. Invest. Radiol. 2006, 41, 15-21.
43. Kothari, M.; Guermazi, A.; White, D.; Suhy, J.; Reinhold, C. Imaging in antiangiogenesis trial: A clinical trials radiology perspective. Br. J. Radiol. 2003, 76, S92-S96.
44. Hsu, C.; Chen, C.N.; Chen, L.T.; Wu, C.Y.; Hsieh, F.J.; Cheng, A.L. Effect of thalidomide in hepatocellular carcinoma: Assessment with power doppler US and analysis of circulating angiogenic factors. Radiology 2005, 235, 509-516.
45. Naugler, W.E.; Sakurai, T.; Kim, S.; Maeda, S.; Kim, K.; Elsharkawy, A.M.; Karin, M. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007, 317, 121-124.
46. Li, Z.P.; Meng, Q.F.; Sun, C.H.; Xu, D.S.; Fan, M.; Yang, X.F.; Chen, D.Y. Tumor angiogenesis and dynamic CT in colorectal carcinoma: Radiologic-pathologic correlation. World J. Gastroenterol. 2005, 11, 1287-1291.
47. Kan, Z.; Phongkitkarun, S.; Kobayashi, S.; Tang, Y.; Ellis, L.M.; Lee, T.Y.; Charnsangavej, C. Functional CT for quantifying tumor perfusion in antiangiogenic therapy in a rat model. Radiology 2005, 237, 151-158.
48. Dvorak, H.F. Vascular permeability factor/vascular endothelial growth factor: A critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 2002, 20, 4368-4380.
49. Wang, J.H.; Min, P.Q.; Wang, P.J.; Cheng, W.X.; Zhang, X.H.; Wang, Y.; Zhao, X.H.; Mao, X.Q. Dynamic CT evaluation of tumor vascularity in renal cell carcinoma. AJR Am. J. Roentgenol. 2006, 186, 1423-1430.
50. Bhatt, R.S.; Seth, P.; Sukhatme, V.P. Biomarkers for monitoring antiangiogenic therapy. Clin. Cancer Res. 2007, 13, 777s-780s.
51. Bruix, J.; Sherman, M.; Llovet, J.M.; Beaugrand, M.; Lencioni, R.; Burroughs, A.K.; Christensen, E.; Pagliaro, L.; Colombo, M.; Rodes, J. Clinical management of hepatocellular carcinoma. Conclusions of the barcelona-2000 EASL conference. European association for the study of the liver. J. Hepatol. 2001, 35, 421-430.
52. Miyazaki, S.; Murase, K.; Yoshikawa, T.; Morimoto, S.; Ohno, Y.; Sugimura, K. A quantitative method for estimating hepatic blood flow using a dual-input single-compartment model. Br. J. Radiol. 2008, 81, 790-800.
53. Materne, R.; Annet, L.; Dechambre, S.; Sempoux, C.; Smith, A.M.; Corot, C.; Horsmans, Y.; vanBeers, B.E. Dynamic computed tomography with low- and high-molecular-mass contrast agents to assess microvascular permeability modifications in a model of liver fibrosis. Clin. Sci. (Lond.) 2002, 103, 213-216.
54. Weidner, N.; Semple, J.P.; Welch, W.R.; Folkman, J. Tumor angiogenesis and metastasis- Correlation in invasive breast carcinoma. N. Engl. J. Med. 1991, 324, 1-8.