Vascular proliferation is associated with survival in pancreatic ductal adenocarcinoma

APMIS

Volumn 121, Issue 11, 2013, Pages 1037-1046

  Hoem, Dag ^a   Straume, Oddbjørn ^a,b   Immervoll, Heike ^b,c   Akslen, Lars A ^a,b   Molven, Anders ^a,b  

^a HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c Alesund Hospital   (Norway)

Author keywords

Angiogenesis; GMP; KRAS mutation; MVD; Pancreatic cancer; Survival; VPI

Indexed keywords

ADULT; AGED; ANGIOGENESIS; ARTICLE; BLOOD VESSEL PARAMETERS; CANCER LOCALIZATION; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SIZE; CANCER SURGERY; CANCER SURVIVAL; CAPILLARY DENSITY; DISEASE ASSOCIATION; FEMALE; GENE MUTATION; GLOMERULOID MICROVASCULAR PROLIFERATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIVER METASTASIS; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MEDICAL RECORD REVIEW; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; POSTOPERATIVE PERIOD; PRIMARY TUMOR; PRIORITY JOURNAL; VASCULAR PROLIFERATION INDEX;

ANGIOGENESIS; GMP; KRAS MUTATION; MVD; PANCREATIC CANCER; SURVIVAL; VPI;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, PANCREATIC DUCTAL; CELL PROLIFERATION; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS;

EID: 84886261782     PISSN: 09034641     EISSN: 16000463     Source Type: Journal    
DOI: 10.1111/apm.12057     Document Type: Article

References (43)

1. Acker T, Plate KH. Role of hypoxia in tumor angiogenesis-molecular and cellular angiogenic crosstalk. Cell Tissue Res 2003;314:145-55.
2. Khorana AA, Ahrendt SA, Ryan CK, Francis CW, Hruban RH, Hu YC, et al. Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin Cancer Res 2007;13:2870-5.
3. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6.
4. Folkman J. Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N Engl J Med 1995;333:1757-63.
5. Persano L, Crescenzi M, Indraccolo S. Anti-angiogenic gene therapy of cancer: current status and future prospects. Mol Aspects Med 2007;28:87-114.
6. Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 1991;324:1-8.
7. Ikeda N, Adachi M, Taki T, Huang C, Hashida H, Takabayashi A, et al. Prognostic significance of angiogenesis in human pancreatic cancer. Br J Cancer 1999;79:1553-63.
8. Pepper MS. Lymphangiogenesis and tumor metastasis: myth or reality? Clin Cancer Res 2001;7:462-8.
9. Benjamin LE, Golijanin D, Itin A, Pode D, Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 1999;103:159-65.
10. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res 2000;60:1388-93.
11. Young RJ, Reed MW. Anti-angiogenic therapy: concept to clinic. Microcirculation 2012;19:115-25.
12. Quesada AR, Munoz-Chapuli R, Medina MA. Anti-angiogenic drugs: from bench to clinical trials. Med Res Rev 2006;26:483-530.
13. Carpelan-Holmström M, Nordling S, Pukkala E, Sankila R, Lüttges J, Klöppel G, et al. Does anyone survive pancreatic ductal adenocarcinoma? A nationwide study re-evaluating the data of the Finnish Cancer Registry Gut 2005;54:385-7.
14. Norwegian Cancer Registry. Cancer in Norway 2009 - Cancer Incidence, Mortality, Survival and Prevalence in Norway. Oslo, Norway: Cancer Registry of Norway, 2011.
15. Neoptolemos JP, Dunn JA, Stocken DD, Almond J, Link K, Beger H, et al. Adjuvant chemoradiotherapy and chemotherapy in resectable pancreatic cancer: a randomised controlled trial. Lancet 2001;358:1576-85.
16. Neoptolemos JP, Stocken DD, Friess H, Bassi C, Dunn JA, Hickey H, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med 2004;350:1200-10.
17. Alexakis N, Halloran C, Raraty M, Ghaneh P, Sutton R, Neoptolemos JP. Current standards of surgery for pancreatic cancer. Br J Surg 2004;91:1410-27.
18. Rausch V, Liu L, Kallifatidis G, Baumann B, Mattern J, Gladkich J, et al. Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res 2010;70:5004-13.
19. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005;69(Suppl 3):4-10.
20. Kerbel RS. Tumor angiogenesis. N Engl J Med 2008;358:2039-49.
21. van der Zee JA, van Eijck CH, Hop WC, van Dekken H, Dicheva BM, Seynhaeve AL, et al. Angiogenesis: a prognostic determinant in pancreatic cancer? Eur J Cancer 2011;47:2576-84.
22. Matsuo Y, Campbell PM, Brekken RA, Sung B, Ouellette MM, Fleming JB, et al. K-Ras promotes angiogenesis mediated by immortalized human pancreatic epithelial cells through mitogen-activated protein kinase signaling pathways. Mol Cancer Res 2009;7:799-808.
23. Banerjee SK, Zoubine MN, Mullick M, Weston AP, Cherian R, Campbell DR. Tumor angiogenesis in chronic pancreatitis and pancreatic adenocarcinoma: impact of K-ras mutations. Pancreas 2000;20:248-55.
24. Straume O, Chappuis PO, Salvesen HB, Halvorsen OJ, Haukaas SA, Goffin JR, et al. Prognostic importance of glomeruloid microvascular proliferation indicates an aggressive angiogenic phenotype in human cancers. Cancer Res 2002;62:6808-11.
25. Goffin JR, Straume O, Chappuis PO, Brunet JS, Begin LR, Hamel N, et al. Glomeruloid microvascular proliferation is associated with p53 expression, germline BRCA1 mutations and an adverse outcome following breast cancer. Br J Cancer 2003;89:1031-4.
26. Tanaka F, Oyanagi H, Takenaka K, Ishikawa S, Yanagihara K, Miyahara R, et al. Glomeruloid microvascular proliferation is superior to intratumoral microvessel density as a prognostic marker in non-small cell lung cancer. Cancer Res 2003;63:6791-4.
27. Immervoll H, Hoem D, Sakariassen PØ, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 2008;8:48.
28. Stefansson IM, Salvesen HB, Akslen LA. Vascular proliferation is important for clinical progress of endometrial cancer. Cancer Res 2006;66:3303-9.
29. Rojiani AM, Dorovini-Zis K. Glomeruloid vascular structures in glioblastoma multiforme: an immunohistochemical and ultrastructural study. J Neurosurg 1996;85:1078-84.
30. Brat DJ, Van Meir EG. Glomeruloid microvascular proliferation orchestrated by VPF/VEGF: a new world of angiogenesis research. Am J Pathol 2001;158:789-96.
31. Sundberg C, Nagy JA, Brown LF, Feng D, Eckelhoefer IA, Manseau EJ, et al. Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am J Pathol 2001;158:1145-60.
32. Immervoll H, Hoem D, Kugarajh K, Steine SJ, Molven A. Molecular analysis of the EGFR-RAS-RAF pathway in pancreatic ductal adenocarcinomas: lack of mutations in the BRAF and EGFR genes. Virchows Arch 2006;448:788-96.
33. Hartwig W, Hackert T, Hinz U, Gluth A, Bergmann F, Strobel O, et al. Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg 2011;254:311-9.
34. Fujimoto K, Hosotani R, Wada M, Lee JU, Koshiba T, Miyamoto Y, et al. Expression of two angiogenic factors, vascular endothelial growth factor and platelet-derived endothelial cell growth factor in human pancreatic cancer, and its relationship to angiogenesis. Eur J Cancer 1998;34:1439-47.
35. Karademir S, Sökmen S, Terzi C, Saǧol O, Ozer E, Astarcioǧlu H, et al. Tumor angiogenesis as a prognostic predictor in pancreatic cancer. J Hepatobiliary Pancreat Surg 2000;7:489-95.
36. Ikeda N, Nakajima Y, Sho M, Adachi M, Huang CL, Iki K, et al. The association of K-ras gene mutation and vascular endothelial growth factor gene expression in pancreatic carcinoma. Cancer 2001;92:488-99.
37. Arnes JB, Stefansson IM, Straume O, Baak JP, Lønning PE, Foulkes WD, et al. Vascular proliferation is a prognostic factor in breast cancer. Breast Cancer Res Treat 2012;133:501-10.
38. Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA. Proliferation of immature tumor vessels is a novel marker of clinical progression in prostate cancer. Cancer Res 2009;69:4708-15.
39. Foulkes WD, Brunet JS, Stefansson IM, Straume O, Chappuis PO, Begin LR, et al. The prognostic implication of the basal-like (cyclin E high/p27 low/p53 + /glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res 2004;64:830-5.
40. Seo Y, Baba H, Fukuda T, Takashima M, Sugimachi K. High expression of vascular endothelial growth factor is associated with liver metastasis and a poor prognosis for patients with ductal pancreatic adenocarcinoma. Cancer 2000;88:2239-45.
41. Kawesha A, Ghaneh P, Andren-Sandberg A, Ogræid D, Skar R, Dawiskiba S, et al. K-ras oncogene subtype mutations are associated with survival but not expression of p53, p16(INK4A), p21(WAF-1), cyclin D1, erbB-2 and erbB-3 in resected pancreatic ductal adenocarcinoma. Int J Cancer 2000;89:469-74.
42. Tsao MS, Liu N, Nicklee T, Shepherd F, Viallet J. Angiogenesis correlates with vascular endothelial growth factor expression but not with Ki-ras oncogene activation in non-small cell lung carcinoma. Clin Cancer Res 1997;3:1807-14.
43. Baba Y, Nosho K, Shima K, Irahara N, Chan AT, Meyerhardt JA, et al. HIF1A overexpression is associated with poor prognosis in a cohort of 731 colorectal cancers. Am J Pathol 2010;176:2292-301.