Microvascular density as an independent predictor of clinical outcome in renal cell carcinoma: An automated image analysis study

Laboratory Investigation

Volumn 92, Issue 1, 2012, Pages 46-56

  Iakovlev, Vladimir V ^a,b   Gabril, Manal ^c   Dubinski, William ^a,b   Scorilas, Andreas ^d   Youssef, Youssef M ^b   Faragalla, Hala ^a,b   Kovacs, Kalman ^a   Rotondo, Fabio ^a   Metias, Shereen ^a   Arsanious, Androu ^a   Plotkin, Anna ^a,b   Girgis, Andrew H F ^a   Streutker, Catherine J ^a,b   Yousef, George M ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c LONDON HEALTH SCIENCES CENTRE   (Canada)

^d UNIVERSITY OF ATHENS   (Greece)

Author keywords

CD34; image analysis; kidney cancer; microvascular density; renal cell carcinoma; tumor vascularity; VEGF

Indexed keywords

CD34 ANTIGEN; VASCULOTROPIN;

ADULT; AGED; AGGRESSIVENESS; ARTICLE; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; KIDNEY CARCINOMA; KIDNEY MEDULLA; LOG RANK TEST; MAJOR CLINICAL STUDY; MALE; MULTIVARIATE ANALYSIS; PRIORITY JOURNAL; PROPORTIONAL HAZARDS MODEL; TUMOR VASCULARIZATION; UNIVARIATE ANALYSIS;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, RENAL CELL; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; TREATMENT OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84855252100     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.153     Document Type: Article

References (68)

1. Srigley JR, Delahunt B. Uncommon and recently described renal carcinomas. Mod Pathol 2009;22(Suppl 2):S2-S23.
2. Weiss RH, Lin PY. Kidney cancer: identification of novel targets for therapy. Kidney Int 2006;69:224-232. (Pubitemid 43323071)
3. Lam JS, Shvarts O, Leppert JT, et al. Postoperative surveillance protocol for patients with localized and locally advanced renal cell carcinoma based on a validated prognostic nomogram and risk group stratification system. J Urol 2005;174:466-472. (Pubitemid 40981575)
4. Antonelli A, Cozzoli A, Zani D, et al. The follow-up management of non-metastatic renal cell carcinoma: definition of a surveillance protocol. BJU Int 2007;99:296-300. (Pubitemid 46103107)
5. Hofmann HS, Neef H, Krohe K, et al. Prognostic factors and survival after pulmonary resection of metastatic renal cell carcinoma. Eur Urol 2005;48:77-81. (Pubitemid 40835595)
6. Klatte T, Patard JJ, Wunderlich H, et al. Metachronous bilateral renal cell carcinoma: risk assessment, prognosis and relevance of the primary-free interval. J Urol 2007;177:2081-2086.
7. Amin MB, Tamboli P, Javidan J, et al. Prognostic impact of histologic subtyping of adult renal epithelial neoplasms: an experience of 405 cases. Am J Surg Pathol 2002;26:281-291. (Pubitemid 34184451)
8. Motzer RJ, Mazumdar M, Bacik J, et al. Survival and prognostic stratification of 670 patients with advanced renal cell carcinoma. J Clin Oncol 1999;17:2530-2540. (Pubitemid 29368255)
9. Mekhail TM, Abou-Jawde RM, Boumerhi G, et al. Validation and extension of the Memorial Sloan-Kettering prognostic factors model for survival in patients with previously untreated metastatic renal cell carcinoma. J Clin Oncol 2005;23:832-841. (Pubitemid 46224183)
10. Thompson RH, Kwon ED. Significance of B7-H1 overexpression in kidney cancer. Clin Genitourin Cancer 2006;5:206-211. (Pubitemid 46190382)
11. Hoffmann NE, Sheinin Y, Lohse CM, et al. External validation of IMP3 expression as an independent prognostic marker for metastatic progression and death for patients with clear cell renal cell carcinoma. Cancer 2008;112:1471-1479. (Pubitemid 351441159)
12. Atkins M, Regan M, McDermott D, et al. Carbonic anhydrase IX expression predicts outcome of interleukin 2 therapy for renal cancer. Clin Cancer Res 2005;11:3714-3721. (Pubitemid 40685588)
13. Arsanious A, Bjarnason GA, Yousef GM. From bench to bedside: current and future applications of molecular profiling in renal cell carcinoma. Mol Cancer 2009;8:20.
14. Chow TF, Youssef YM, Lianidou E, et al. Differential expression profiling of microRNAs and their potential involvement in renal cell carcinoma pathogenesis. Clin Biochem 2010;43:150-158.
15. Lam JS, Pantuck AJ, Belldegrun AS, et al. Protein expression profiles in renal cell carcinoma: staging, prognosis, and patient selection for clinical trials. Clin Cancer Res 2007;13(2 Pt 2):703s-708s.
16. Romaschin AD, Youssef Y, Chow TF, et al. Exploring the pathogenesis of renal cell carcinoma: pathway and bioinformatics analysis of dysregulated genes and proteins. Biol Chem 2009;390:125-135.
17. Schaefer A, Stephan C, Busch J, et al. Diagnostic, prognostic and therapeutic implications of microRNAs in urologic tumors. Nat Rev Urol 2010;7:286-297.
18. Siu KW, DeSouza LV, Scorilas A, et al. Differential protein expressions in renal cell carcinoma: new biomarker discovery by mass spectrometry. J Proteome Res 2009;8:3797-3807.
19. Bosari S, Lee AK, DeLellis RA, et al. Microvessel quantitation and prognosis in invasive breast carcinoma. Hum Pathol 1992;23: 755-761.
20. Brem S, Cotran R, Folkman J. Tumor angiogenesis: a quantitative method for histologic grading. J Natl Cancer Inst 1972;48: 347-356.
21. Weidner N, Folkman J, Pozza F, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 1992;84:1875-1887. (Pubitemid 23004615)
22. Weidner N, Carroll PR, Flax J, et al. Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am J Pathol 1993;143: 401-409. (Pubitemid 24058195)
23. Schoell WM, Pieber D, Reich O, et al. Tumor angiogenesis as a prognostic factor in ovarian carcinoma: quantification of endothelial immunoreactivity by image analysis. Cancer 1997;80:2257-2262. (Pubitemid 28007396)
24. Imao T, Egawa M, Takashima H, et al. Inverse correlation of microvessel density with metastasis and prognosis in renal cell carcinoma. Int J Urol 2004;11:948-953. (Pubitemid 39577188)
25. Maclennan GT, Bostwick DG. Microvessel density in renal cell carcinoma: lack of prognostic significance. Urology 1995;46:27-30.
26. Minardi D, Lucarini G, Mazzucchelli R, et al. Prognostic role of Fuhrman grade and vascular endothelial growth factor in pT1a clear cell carcinoma in partial nephrectomy specimens. J Urol 2005;174(4 Pt 1): 1208-1212. (Pubitemid 41318683)
27. Nativ O, Sabo E, Reiss A, et al. Clinical significance of tumor angiogenesis in patients with localized renal cell carcinoma. Urology 1998;51:693-696. (Pubitemid 28261919)
28. Sabo E, Boltenko A, Sova Y, et al. Microscopic analysis and significance of vascular architectural complexity in renal cell carcinoma. Clin Cancer Res 2001;7:533-537. (Pubitemid 32707975)
29. Sandlund J, Hedberg Y, Bergh A, et al. Evaluation of CD31 (PECAM-1) expression using tissue microarray in patients with renal cell carcinoma. Tumour Biol 2007;28:158-164. (Pubitemid 46976002)
30. Yildiz E, Ayan S, Goze F, et al. Relation of microvessel density with microvascular invasion, metastasis and prognosis in renal cell carcinoma. BJU Int 2008;101:758-764. (Pubitemid 351270001)
31. Yoshino S, Kato M, Okada K. Prognostic significance of microvessel count in low stage renal cell carcinoma. Int J Urol 1995;2:156-160.
32. Ahlgren J, Risberg B, Villman K, et al. Angiogenesis in invasive breast carcinoma-a prospective study of tumour heterogeneity. Eur J Cancer 2002;38:64-69. (Pubitemid 34031827)
33. Fox SB, Harris AL. Histological quantitation of tumour angiogenesis. APMIS 2004;112:413-430. (Pubitemid 39626050)
34. 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;94:883-893. (Pubitemid 34778087)
35. Lee AH. The relationship of vascularity of the primary tumour to lymph node metastases and to distant haematogenous spread in carcinoma of the breast. Histopathology 2002;41:366-368. (Pubitemid 35279037)
36. Sharma S, Sharma MC, Sarkar C. Morphology of angiogenesis in human cancer: a conceptual overview, histoprognostic perspective and significance of neoangiogenesis. Histopathology 2005;46:481-489. (Pubitemid 40632304)
37. Couvelard A, O'Toole D, Turley H, et al. Microvascular density and hypoxia-inducible factor pathway in pancreatic endocrine tumours: negative correlation of microvascular density and VEGF expression with tumour progression. Br J Cancer 2005;92:94-101. (Pubitemid 40188441)
38. Bartoletti R, Cai T, Nesi G, et al. Qualitative and quantitative analysis of angiogenetic factors in transitional cell bladder carcinoma: relationship with clinical course at 10 years follow-up. Oncol Rep 2005;14:251-255.
39. Hoskin PJ, Sibtain A, Daley FM, et al. The immunohistochemical assessment of hypoxia, vascularity and proliferation in bladder carcinoma. Radiother Oncol 2004;72:159-168. (Pubitemid 39024591)
40. Kaanders JH, Wijffels KI, Marres HA, et al. Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Res 2002;62:7066-7074. (Pubitemid 35424102)
41. Dagnon K, Heudes D, Bernaudin JF, et al. Computerized morphometric analysis of microvasculature in non-small cell lung carcinoma. Microvasc Res 2008;75:112-118. (Pubitemid 350266731)
42. Yuan A, Yang PC, Yu CJ, et al. Tumor angiogenesis correlates with histologic type and metastasis in non-small-cell lung cancer. Am J Respir Crit Care Med 1995;152(6 Pt 1):2157-2162. (Pubitemid 3019578)
43. Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 1990;82:4-6. (Pubitemid 20020880)
44. Trivella M, Pezzella F, Pastorino U, et al. Microvessel density as a prognostic factor in non-small-cell lung carcinoma: a meta-analysis of individual patient data. Lancet Oncol 2007;8:488-499. (Pubitemid 46805904)
45. Chalkley HW. Method for the quantitative morphologic analysis of tissues. J Natl Cancer Inst 1943;4:47-53.
46. Hansen S, Grabau DA, Rose C, et al. Angiogenesis in breast cancer: a comparative study of the observer variability of methods for determining microvessel density. Lab Invest 1998;78:1563-1573. (Pubitemid 29022232)
47. Motzer RJ, Rini BI, Bukowski RM, et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006;295:2516-2524. (Pubitemid 43854967)
48. Ratain MJ, Eisen T, Stadler WM, et al. Phase II placebo-controlled randomized discontinuation trial of sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol 2006;24:2505-2512. (Pubitemid 46630627)
49. Kerbel RS. Tumor angiogenesis: past, present and the near future. Carcinogenesis 2000;21:505-515. (Pubitemid 30137936)
50. Stadler WM, Kuzel T, Shapiro C, et al. Multi-institutional study of the angiogenesis inhibitor TNP-470 in metastatic renal carcinoma. J Clin Oncol 1999;17:2541-2545. (Pubitemid 29368256)
51. Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 2003;349:427-434. (Pubitemid 36910021)
52. Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 1982;6:655-663. (Pubitemid 13234762)
53. Iakovlev VV, Pintilie M, Morrison A, et al. Effect of distributional heterogeneity on the analysis of tumor hypoxia based on carbonic anhydrase IX. Lab Invest 2007;87:1206-1217. (Pubitemid 350126705)
54. Hedley D, Pintilie M, Woo J, et al. Carbonic anhydrase IX expression, hypoxia, and prognosis in patients with uterine cervical carcinomas. Clin Cancer Res 2003;9:5666-5674. (Pubitemid 37499489)
55. Hedley D, Pintilie M, Woo J, et al. Up-regulation of the redox mediators thioredoxin and apurinic/apyrimidinic excision (APE)/Ref-1 in hypoxic microregions of invasive cervical carcinomas, mapped using multispectral, wide-field fluorescence image analysis. Am J Pathol 2004;164:557-565. (Pubitemid 38364671)
56. Pham NA, Morrison A, Schwock J, et al. Quantitative image analysis of immunohistochemical stains using a CMYK color model. Diagn Pathol 2007;2:8.
57. Pintilie M, Iakovlev V, Fyles A, et al. Heterogeneity and power in clinical biomarker studies. J Clin Oncol 2009;27:1517-1521.
58. Dome B, Hendrix MJ, Paku S, et al. Alternative vascularization mechanisms in cancer: pathology and therapeutic implications. Am J Pathol 2007;170:1-15. (Pubitemid 47339184)
59. Benjamin LE, Golijanin D, Itin A, et al. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 1999;103: 159-165. (Pubitemid 29053133)
60. Baldewijns MM, van Vlodrop IJ, Vermeulen PB, et al. VHL and HIF signalling in renal cell carcinogenesis. J Pathol 2010;221:125-138.
61. Flaherty KT, Puzanov I. Building on a foundation of VEGF and mTOR targeted agents in renal cell carcinoma. Biochem Pharmacol 2010;80:638-646.
62. de la Taille A, Katz AE, Bagiella E, et al. Microvessel density as a predictor of PSA recurrence after radical prostatectomy. A comparison of CD34 and CD31. Am J Clin Pathol 2000;113:555-562. (Pubitemid 30217365)
63. Kato T, Kameoka S, Kimura T, et al. The combination of angiogenesis and blood vessel invasion as a prognostic indicator in primary breast cancer. Br J Cancer 2003;88:1900-1908. (Pubitemid 36829665)
64. Mineo TC, Ambrogi V, Baldi A, et al. Prognostic impact of VEGF, CD31, CD34, and CD105 expression and tumour vessel invasion after radical surgery for IB-IIA non-small cell lung cancer. J Clin Pathol 2004;57:591-597. (Pubitemid 38725758)
65. Qian CN, Min HQ, Liang XM, et al. Primary study of neovasculature correlating with metastatic nasopharyngeal carcinoma using computer image analysis. J Cancer Res Clin Oncol 1997;123:645-651.
66. Tanaka F, Otake Y, Yanagihara K, et al. Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res 2001;7:3410-3415. (Pubitemid 33069974)
67. Baldewijns MM, Thijssen VL, Van den Eynden GG, et al. High-grade clear cell renal cell carcinoma has a higher angiogenic activity than low-grade renal cell carcinoma based on histomorphological quantification and qRT-PCR mRNA expression profile. Br J Cancer 2007;96:1888-1895. (Pubitemid 46912016)
68. Sandlund J, Hedberg Y, Bergh A, et al. Endoglin (CD105) expression in human renal cell carcinoma. BJU Int 2006;97:706-710. (Pubitemid 43383499)