Prognostic value of carbonic anhydrase ix immunohistochemical expression in renal cell carcinoma: A meta-analysis of the literature

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Zhao, Zhihong ^a   Liao, Guixiang ^b   Li, Yongqiang ^a   Zhou, Shulu ^a   Zou, Hequn ^a   Ferno, Samitha ^c  

^a THE THIRD AFFILIATED HOSPITAL OF SOUTHERN MEDICAL UNIVERSITY   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE IX; TUMOR MARKER; CA9 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; TUMOR ANTIGEN;

ARTICLE; BRAZIL; CANCER GRADING; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; DISEASE FREE SURVIVAL; DISTANT METASTASIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FRANCE; GERMANY; HAZARD RATIO; HUMAN; IMMUNOHISTOCHEMISTRY; JAPAN; KIDNEY CARCINOMA; KOREA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; META ANALYSIS; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SPAIN; SWEDEN; SYSTEMATIC REVIEW; TUMOR INVASION; TURKEY (REPUBLIC); UNITED KINGDOM; UNITED STATES; CARCINOMA, RENAL CELL; KIDNEY; KIDNEY NEOPLASMS; LYMPHATIC METASTASIS; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS;

ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CARBONIC ANHYDRASES; CARCINOMA, RENAL CELL; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY NEOPLASMS; LYMPHATIC METASTASIS; PROGNOSIS; SURVIVAL ANALYSIS;

EID: 84913528977     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114096     Document Type: Article

References (76)

1. Koul H, Huh JS, Rove KO, Crompton L, Koul S, et al. (2011) Molecular aspects of renal cell carcinoma: a review. Am J Cancer Res 1: 240-254.
2. Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64: 9-29.
3. Mocellin S, Zavagno G, Nitti D (2008) The prognostic value of serum S100B in patients with cutaneous melanoma: a meta-analysis. Int J Cancer 123: 2370-2376.
4. Di Napoli A, Signoretti S (2009) Tissue biomarkers in renal cell carcinoma: issues and solutions. Cancer 115: 2290-2297.
5. Brunelli M, Eccher A, Gobbo S, Ficarra V, Novara G, et al. (2008) Loss of chromosome 9p is an independent prognostic factor in patients with clear cell renal cell carcinoma. Mod Pathol 21: 1-6.
6. Parker AS, Leibovich BC, Lohse CM, Sheinin Y, Kuntz SM, et al. (2009) Development and evaluation of BioScore: a biomarker panel to enhance prognostic algorithms for clear cell renal cell carcinoma. Cancer 115: 2092-2103.
7. Joseph RW, Kapur P, Serie DJ, Eckel-Passow JE, Parasramka M, et al. (2014) Loss of BAP1 protein expression is an independent marker of poor prognosis in patients with low-risk clear cell renal cell carcinoma. Cancer 120: 1059-1067.
8. Da CW, Rezende M, Carneiro FC, Rocha RM, Da CI, et al. (2014) Polybromo-1 (PBRM1), a SWI/SNF complex subunit is a prognostic marker in clear cell renal cell carcinoma. BJU Int 113: E157-E163.
9. Zhang Y, Sun B, Zhao X, Liu Z, Wang X, et al. (2013) Clinical significances and prognostic value of cancer stem-like cells markers and vasculogenic mimicry in renal cell carcinoma. J Surg Oncol 108: 414-419.
10. Jiang Z, Chu PG, Woda BA, Rock KL, Liu Q, et al. (2006) Analysis of RNA-binding protein IMP3 to predict metastasis and prognosis of renal-cell carcinoma: a retrospective study. Lancet Oncol 7: 556-564.
11. Pastorekova S, Zavadova Z, Kostal M, Babusikova O, Zavada J (1992) A novel quasi-viral agent, MaTu, is a two-component system. Virology 187: 620-626.
12. Potter C, Harris AL (2004) Hypoxia inducible carbonic anhydrase IX, marker of tumour hypoxia, survival pathway and therapy target. Cell Cycle 3: 164-167.
13. Thiry A, Dogne JM, Masereel B, Supuran CT (2006) Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 27: 566-573.
14. Xu C, Lo A, Yammanuru A, Tallarico AS, Brady K, et al. (2010) Unique biological properties of catalytic domain directed human anti-CAIX antibodies discovered through phage-display technology. PLoS One 5: e9625.
15. Signoretti S, Regan M, Atkins M (2008) Carbonic anhydrase IX as a predictive biomarker of response to kidney cancer therapy. BJU Int 101 Suppl. 4: 31-35.
16. Choueiri TK, Cheng S, Qu AQ, Pastorek J, Atkins MB, et al. (2013) Carbonic anhydrase IX as a potential biomarker of efficacy in metastatic clear-cell renal cell carcinoma patients receiving sorafenib or placebo: analysis from the treatment approaches in renal cancer global evaluation trial (TARGET). Urol Oncol 31: 1788-1793.
17. Rasmussen S, Donskov F, Pedersen JW, Wandall HH, Buus S, et al. (2013) Carbon anhydrase IX specific immune responses in patients with metastatic renal cell carcinoma potentially cured by interleukin-2 based immunotherapy. Immunopharmacol Immunotoxicol 35: 487-496.
18. Zhang BY, Thompson RH, Lohse CM, Dronca RS, Cheville JC, et al. (2013) Carbonic anhydrase IX (CAIX) is not an independent predictor of outcome in patients with clear cell renal cell carcinoma (ccRCC) after long-term follow-up. BJU Int 111: 1046-1053.
19. Zerati M, Leite KR, Pontes-Junior J, Segre CC, Reis ST, et al. (2013) Carbonic Anhydrase IX is not a predictor of outcomes in non-metastatic clear cell renal cell carcinoma - a digital analysis of tissue microarray. Int Braz J Urol 39: 484-492.
20. Xing X, Tang YB, Yuan G, Wang Y, Wang J, et al. (2013) The prognostic value of E-cadherin in gastric cancer: a meta-analysis. Int J Cancer 132: 2589-2596.
21. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50: 1088-1101.
22. Krieg A, Werner TA, Verde PE, Stoecklein NH, Knoefel WT (2013) Prognostic and clinicopathological significance of survivin in colorectal cancer: a meta-analysis. PLoS One 8: e65338.
23. Pena C, Lathia C, Shan M, Escudier B, Bukowski RM (2010) Biomarkers predicting outcome in patients with advanced renal cell carcinoma: Results from sorafenib phase III Treatment Approaches in Renal Cancer Global Evaluation Trial. Clin Cancer Res 16: 4853-4863.
24. Sim SH, Messenger MP, Gregory WM, Wind TC, Vasudev NS, et al. (2012) Prognostic utility of preoperative circulating osteopontin, carbonic anhydrase IX and CRP in renal cell carcinoma. Br J Cancer 107: 1131-1137.
25. Zhou GX, Ireland J, Rayman P, Finke J, Zhou M (2010) Quantification of carbonic anhydrase IX expression in serum and tissue of renal cell carcinoma patients using enzyme-linked immunosorbent assay: prognostic and diagnostic potentials. Urology 75: 257-261.
26. Li G, Feng G, Gentil-Perret A, Genin C, Tostain J (2008) Serum carbonic anhydrase 9 level is associated with postoperative recurrence of conventional renal cell cancer. J Urol 180: 510-513, 513-514.
27. Papworth K, Sandlund J, Grankvist K, Ljungberg B, Rasmuson T (2010) Soluble carbonic anhydrase IX is not an independent prognostic factor in human renal cell carcinoma. Anticancer Res 30: 2953-2957.
28. Gigante M, Li G, Ferlay C, Perol D, Blanc E, et al. (2012) Prognostic value of serum CA9 in patients with metastatic clear cell renal cell carcinoma under targeted therapy. Anticancer Res 32: 5447-5451.
29. de la Taille A, Katz A, Cao Y, McKiernan J, Buttyan R, et al. (2000) Blood-based RT-PCR assays of MN/CA9 or PSMA: clinical application in renal cancer patients. Urology 56: 393-398.
30. Li G, Feng G, Gentil-Perret A, Genin C, Tostain J (2007) CA9 gene expression in conventional renal cell carcinoma: a potential marker for prediction of early metastasis after nephrectomy. Clin Exp Metastasis 24: 149-155.
31. Gilbert SM, Whitson JM, Mansukhani M, Buttyan R, Benson MC, et al. (2006) Detection of carbonic anhydrase-9 gene expression in peripheral blood cells predicts risk of disease recurrence in patients with renal cortical tumors. Urology 67: 942-945.
32. Klatte T, Rao PN, de Martino M, LaRochelle J, Shuch B, et al. (2009) Cytogenetic profile predicts prognosis of patients with clear cell renal cell carcinoma. J Clin Oncol 27: 746-753.
33. Girgis AH, Iakovlev VV, Beheshti B, Bayani J, Squire JA, et al. (2012) Multilevel whole-genome analysis reveals candidate biomarkers in clear cell renal cell carcinoma. Cancer Res 72: 5273-5284.
34. de Martino M, Klatte T, Seligson DB, LaRochelle J, Shuch B, et al. (2009) CA9 gene: single nucleotide polymorphism predicts metastatic renal cell carcinoma prognosis. J Urol 182: 728-734.
35. Takacova M, Bartosova M, Skvarkova L, Zatovicova M, Vidlickova I, et al. (2013) Carbonic anhydrase IX is a clinically significant tissue and serum biomarker associated with renal cell carcinoma. Oncol Lett 5: 191-197.
36. Kroeger N, Seligson DB, Klatte T, Rampersaud EN, Birkhauser FD, et al. (2012) Clinical, molecular, and genetic correlates of lymphatic spread in clear cell renal cell carcinoma. Eur Urol 61: 888-895.
37. Lam JS, Shvarts O, Said JW, Pantuck AJ, Seligson DB, et al. (2005) Clinicopathologic and molecular correlations of necrosis in the primary tumor of patients with renal cell carcinoma. Cancer 103: 2517-2525.
38. Yu W, Zhang W, Jiang Y, Wang Y, Li Y, et al. (2013) Clinicopathological, genetic, ultrastructural characterizations and prognostic factors of papillary renal cell carcinoma: new diagnostic and prognostic information. Acta Histochem 115: 452-459.
39. Edeline J, Mottier S, Vigneau C, Jouan F, Perrin C, et al. (2012) Description of 2 angiogenic phenotypes in clear cell renal cell carcinoma. Hum Pathol 43: 1982-1990.
40. Dahinden C, Ingold B, Wild P, Boysen G, Luu VD, et al. (2010) Mining tissue microarray data to uncover combinations of biomarker expression patterns that improve intermediate staging and grading of clear cell renal cell cancer. Clin Cancer Res 16: 88-98.
41. McCormick RI, Blick C, Ragoussis J, Schoedel J, Mole DR, et al. (2013) miR-210 is a target of hypoxia-inducible factors 1 and 2 in renal cancer, regulates ISCU and correlates with good prognosis. Br J Cancer 108: 1133-1142.
42. Cho D, Signoretti S, Dabora S, Regan M, Seeley A, et al. (2007) Potential histologic and molecular predictors of response to temsirolimus in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 5: 379-385.
43. Jensen HK, Donskov F, Marcussen N, Nordsmark M, Lundbeck F, et al. (2009) Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol 27: 4709-4717.
44. Garcia-Donas J, Leandro-Garcia LJ, Gonzalez DAA, Morente M, Alemany I, et al. (2013) Prospective study assessing hypoxia-related proteins as markers for the outcome of treatment with sunitinib in advanced clear-cell renal cell carcinoma. Ann Oncol 24: 2409-2414.
45. Tripodi SA, Del VM, Supuran CT, Scozzafava A, Gabrielli MG, et al. (2004) Redox state and carbonic anhydrase isozyme IX expression in human renal cell carcinoma: biochemical and morphological investigations. J Enzyme Inhib Med Chem 19: 287-291.
46. Dorai T, Sawczuk IS, Pastorek J, Wiernik PH, Dutcher JP (2005) The role of carbonic anhydrase IX overexpression in kidney cancer. Eur J Cancer 41: 2935-2947.
47. Jensen HK, Nordsmark M, Donskov F, Marcussen N, von der Maase H (2008) Immunohistochemical expression of carbonic anhydrase IX assessed over time and during treatment in renal cell carcinoma. BJU Int 101 Suppl. 4: 41-44.
48. Bui MH, Visapaa H, Seligson D, Kim H, Han KR, et al. (2004) Prognostic value of carbonic anhydrase IX and KI67 as predictors of survival for renal clear cell carcinoma. J Urol 171: 2461-2466.
49. Kim HL, Seligson D, Liu X, Janzen N, Bui MH, et al. (2005) Using tumor markers to predict the survival of patients with metastatic renal cell carcinoma. J Urol 173: 1496-1501.
50. Leibovich BC, Sheinin Y, Lohse CM, Thompson RH, Cheville JC, et al. (2007) Carbonic anhydrase IX is not an independent predictor of outcome for patients with clear cell renal cell carcinoma. J Clin Oncol 25: 4757-4764.
51. Muriel LC, Esteban E, Astudillo A, Pardo P, Berros JP, et al. (2012) Predictive factors for response to treatment in patients with advanced renal cell carcinoma. Invest New Drugs 30: 2443-2449.
52. Kim HL, Seligson D, Liu X, Janzen N, Bui MH, et al. (2004) Using protein expressions to predict survival in clear cell renal carcinoma. Clin Cancer Res 10: 5464-5471.
53. Eckel-Passow JE, Lohse CM, Sheinin Y, Crispen PL, Krco CJ, et al. (2010) Tissue microarrays: one size does not fit all. Diagn Pathol 5: 48.
54. Klatte T, Pantuck AJ, Said JW, Seligson DB, Rao NP, et al. (2009) Cytogenetic and molecular tumor profiling for type 1 and type 2 papillary renal cell carcinoma. Clin Cancer Res 15: 1162-1169.
55. Klatte T, Seligson DB, LaRochelle J, Shuch B, Said JW, et al. (2009) Molecular signatures of localized clear cell renal cell carcinoma to predict disease-free survival after nephrectomy. Cancer Epidemiol Biomarkers Prev 18: 894-900.
56. Shvarts O, Seligson D, Lam J, Shi T, Horvath S, et al. (2005) p53 is an independent predictor of tumor recurrence and progression after nephrectomy in patients with localized renal cell carcinoma. J Urol 173: 725-728.
57. Atkins M, Regan M, McDermott D, Mier J, Stanbridge E, et al. (2005) Carbonic anhydrase IX expression predicts outcome of interleukin 2 therapy for renal cancer. Clin Cancer Res 11: 3714-3721.
58. Biswas S, Charlesworth PJ, Turner GD, Leek R, Thamboo PT, et al. (2012) CD31 angiogenesis and combined expression of HIF-1alpha and HIF-2alpha are prognostic in primary clear-cell renal cell carcinoma (CC-RCC), but HIFalpha transcriptional products are not: implications for antiangiogenic trials and HIFalpha biomarker studies in primary CC-RCC. Carcinogenesis 33: 1717-1725.
59. Bui MH, Seligson D, Han KR, Pantuck AJ, Dorey FJ, et al. (2003) Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implications for prognosis and therapy. Clin Cancer Res 9: 802-811.
60. Dornbusch J, Zacharis A, Meinhardt M, Erdmann K, Wolff I, et al. (2013) Analyses of potential predictive markers and survival data for a response to sunitinib in patients with metastatic renal cell carcinoma. PLoS One 8: e76386.
61. Dudek AZ, Yee RT, Manivel JC, Isaksson R, Yee HO (2010) Carbonic anhydrase IX expression is associated with improved outcome of high-dose interleukin-2 therapy for metastatic renal cell carcinoma. Anticancer Res 30: 987-992.
62. Kim HS, Kim WS, Park SH, Jung CW, Choi HY, et al. (2010) Molecular biomarkers for advanced renal cell carcinoma: implications for prognosis and therapy. Urol Oncol 28: 157-163.
63. Klatte T, Seligson DB, Riggs SB, Leppert JT, Berkman MK, et al. (2007) Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin Cancer Res 13: 7388-7393.
64. Muriel LC, Esteban E, Berros JP, Pardo P, Astudillo A, et al. (2012) Prognostic factors in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 10: 262-270.
65. Patard JJ, Fergelot P, Karakiewicz PI, Klatte T, Trinh QD, et al. (2008) Low CAIX expression and absence of VHL gene mutation are associated with tumor aggressiveness and poor survival of clear cell renal cell carcinoma. Int J Cancer 123: 395-400.
66. Phuoc NB, Ehara H, Gotoh T, Nakano M, Kamei S, et al. (2008) Prognostic value of the co-expression of carbonic anhydrase IX and vascular endothelial growth factor in patients with clear cell renal cell carcinoma. Oncol Rep 20: 525-530.
67. Sandlund J, Oosterwijk E, Grankvist K, Oosterwijk-Wakka J, Ljungberg B, et al. (2007) Prognostic impact of carbonic anhydrase IX expression in human renal cell carcinoma. BJU Int 100: 556-560.
68. Soyupak B, Erdogan S, Ergin M, Seydaoglu G, Kuzgunbay B, et al. (2005) CA9 expression as a prognostic factor in renal clear cell carcinoma. Urol Int 74: 68-73.
69. Gore ME, Larkin JM (2011) Challenges and opportunities for converting renal cell carcinoma into a chronic disease with targeted therapies. Br J Cancer 104: 399-406.
70. Maroto P, Rini B (2014) Molecular Biomarkers in Advanced Renal Cell Carcinoma. Clin Cancer Res.
71. Ilie M, Hofman V, Zangari J, Chiche J, Mouroux J, et al. (2013) Response of CAIX and CAXII to in vitro re-oxygenation and clinical significance of the combined expression in NSCLC patients. Lung Cancer 82: 16-23.
72. Egger M, Zellweger-Zahner T, Schneider M, Junker C, Lengeler C, et al. (1997) Language bias in randomised controlled trials published in English and German. Lancet 350: 326-329.
73. Choschzick M, Oosterwijk E, Muller V, Woelber L, Simon R, et al. (2011) Overexpression of carbonic anhydrase IX (CAIX) is an independent unfavorable prognostic marker in endometrioid ovarian cancer. Virchows Arch 459: 193-200.
74. Driessen A, Landuyt W, Pastorekova S, Moons J, Goethals L, et al. (2006) Expression of carbonic anhydrase IX (CA IX), a hypoxia-related protein, rather than vascular-endothelial growth factor (VEGF), a pro-angiogenic factor, correlates with an extremely poor prognosis in esophageal and gastric adenocarcinomas. Ann Surg 243: 334-340.
75. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
76. Egger M. Zellweger-Zahner T. Schneider M. Junker C. Lengeler C. et al. 1997 Language bias in randomised controlled trials published in English and German. Lancet 350 326-329