Development of a multimarker assay for early detection of ovarian cancer

Journal of Clinical Oncology

Volumn 28, Issue 13, 2010, Pages 2159-2166

  Yurkovetsky, Zoya ^a   Skates, Steven ^a   Lomakin, Aleksey ^a   Nolen, Brian ^a   Pulsipher, Trenton ^a   Modugno, Francesmary ^a   Marks, Jeffrey ^a   Godwin, Andrew ^a   Gorelik, Elieser ^a   Jacobs, Ian ^a   Menon, Usha ^a   Lu, Karen ^a   Badgwell, Donna ^a   Bast Jr , Robert C ^a   Lokshin, Anna E ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CA 125 ANTIGEN; CARCINOEMBRYONIC ANTIGEN; HUMAN EPIDIDYMIS PROTEIN 4; VASCULAR CELL ADHESION MOLECULE 1; DEFB126 PROTEIN, HUMAN; EPIDIDYMAL SECRETORY PROTEIN; TUMOR MARKER;

ADULT; AGED; ALGORITHM; ARTICLE; CANCER SCREENING; CONTROLLED STUDY; EARLY DIAGNOSIS; FEMALE; HUMAN; IMMUNOASSAY; MAJOR CLINICAL STUDY; MONTE CARLO METHOD; OVARY CANCER; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; VALIDATION PROCESS; BLOOD; CANCER STAGING; COMPARATIVE STUDY; MASS SCREENING; METHODOLOGY; MIDDLE AGED; OVARY TUMOR; PATHOLOGY; PREDICTION AND FORECASTING; PROGNOSIS; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; STATISTICAL ANALYSIS; STATISTICS; VALIDATION STUDY;

AGED; AGED, 80 AND OVER; ALGORITHMS; CA-125 ANTIGEN; CARCINOEMBRYONIC ANTIGEN; DATA INTERPRETATION, STATISTICAL; EARLY DETECTION OF CANCER; EPIDIDYMAL SECRETORY PROTEINS; FEMALE; HUMANS; IMMUNOASSAY; MASS SCREENING; MIDDLE AGED; MONTE CARLO METHOD; NEOPLASM STAGING; OVARIAN NEOPLASMS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TUMOR MARKERS, BIOLOGICAL; VASCULAR CELL ADHESION MOLECULE-1;

EID: 77952315345     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2008.19.2484     Document Type: Article

References (96)

1. Boente MP, Schilder R, Ozols RF: Gynecological cancers. Cancer Chemother Biol Response Modif 18:418-434, 1999
2. Baker TR, Piver MS: Etiology, biology, and epidemiology of ovarian cancer. Semin Surg Oncol 10:242-248, 1994
3. Holschneider CH, Berek JS: Ovarian cancer: Epidemiology, biology, and prognostic factors. Semin Surg Oncol 19:3-10, 2000 (Pubitemid 30439309)
4. Jacobs I, Bast RC Jr: The CA 125 tumour-associated antigen: A review of the literature. Hum Reprod 4:1-12, 1989 (Pubitemid 19069900)
5. van Haaften-Day C, Shen Y, Xu F, et al: OVX1, macrophage-colony stimulating factor, and CA-125-II as tumor markers for epithelial ovarian carcinoma: A critical appraisal. Cancer 92:2837-2844, 2001 (Pubitemid 33091920)
6. Woolas RP, Xu FJ, Jacobs IJ, et al: Elevation of multiple serum markers in patients with stage I ovarian cancer. J Natl Cancer Inst 85:1748-1751, 1993 (Pubitemid 23320845)
7. Chi DS, Hoskins WJ: Ovarian cancer controversy: When and how to use available screening methods. Medscape Womens Health 1:3, 1996
8. DePriest PD, DeSimone CP: Ultrasound screening for the early detection of ovarian cancer. J Clin Oncol 21:194-199, 2003 (suppl 10)
9. MacDonald ND, Rosenthal AN, Jacobs IJ: Screening for ovarian cancer. Ann Acad Med Singapore 27:676-682, 1998
10. Menon U, Jacobs IJ: Ovarian cancer screening in the general population. Curr Opin Obstet Gynecol 13:61-64, 2001 (Pubitemid 32667437)
11. Jacobs IJ, Menon U: Progress and challenges in screening for early detection of ovarian cancer. Mol Cell Proteomics 3:355-366, 2004 (Pubitemid 38702089)
12. Baron AT, Lafky JM, Boardman CH, et al: Serum sErbB1 and epidermal growth factor levels as tumor biomarkers in women with stage III or IV epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev 8:129-137, 1999 (Pubitemid 29085379)
13. Baron AT, Cora EM, Lafky JM, et al: Soluble epidermal growth factor receptor (sEGFR/sErbB1) as a potential risk, screening, and diagnostic serum biomarker of epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev 12:103-113, 2003 (Pubitemid 36193999)
14. Mazurek A, Niklinski J, Laudanski T, et al: Clinical tumour markers in ovarian cancer. Eur J Cancer Prev 7:23-35, 1998 (Pubitemid 28164133)
15. Hasholzner U, Baumgartner L, Stieber P, et al: Significance of the tumour markers CA 125 II, CA 72-4, CASA and CYFRA 21-1 in ovarian carcinoma. Anticancer Res 14:2743-2746, 1994
16. Perkins GL, Slater ED, Sanders GK, et al: Serum tumor markers. Am Fam Physician 68:1075-1082, 2003 (Pubitemid 37173829)
17. Skates SJ, Horick N, Yu Y, et al: Preoperative sensitivity and specificity for early-stage ovarian cancer when combining cancer antigen CA-125II, CA 15-3, CA 72-4, and macrophage colony-stimulating factor using mixtures of multivariate normal distributions. J Clin Oncol 22:4059-4066, 2004 (Pubitemid 41185174)
18. Zhang Z, Bast RC Jr, Yu Y, et al: Three biomarkers identified from serum proteomic analysis for the detection of early stage ovarian cancer. Cancer Res 64:5882-5890, 2004 (Pubitemid 39095590)
19. Visintin I, Feng Z, Longton G, et al: Diagnostic markers for early detection of ovarian cancer. Clin Cancer Res 14:1065-1072, 2008 (Pubitemid 351302552)
20. Yurkovetsky Z, Ta'asan S, Skates S, et al: Development of multimarker panel for early detection of endometrial cancer: High diagnostic power of prolactin. Gynecol Oncol 107:58-65, 2007 (Pubitemid 47464542)
21. Gorelik E, Landsittel DP, Marrangoni AM, et al: Multiplexed immunobead-based cytokine profiling for early detection of ovarian cancer. Cancer Epidemiol Biomarkers Prev 14:981-987, 2005 (Pubitemid 40478567)
22. Gallagher NJ, Eliopoulos AG, Agathangelo A, et al: CD40 activation in epithelial ovarian carcinoma cells modulates growth, apoptosis, and cytokine secretion. Mol Pathol 55:110-120, 2002 (Pubitemid 34293413)
23. Merritt WM, Sood AK: Markers of angiogenesis in ovarian cancer. Dis Markers 23:419-431, 2007 (Pubitemid 350171264)
24. Maihle NJ, Baron AT, Barrette BA, et al: EGF/ErbB receptor family in ovarian cancer. Cancer Treat Res 107:247-258, 2002
25. Cheung TH, Wong YF, Chung TK, et al: Clinical use of serum c-erbB-2 in patients with ovarian masses. Gynecol Obstet Invest 48:133-137, 1999 (Pubitemid 29397126)
26. Marx D, Fattahi-Meibodi A, Kudelka R, et al: Detection of p105 (c-erbB-2, HER2/neu) serum levels by a new ELISA in patients with ovarian carcinoma. Anticancer Res 18:2891-2894, 1998 (Pubitemid 28388858)
27. Schoen RE, Weissfeld JL, Kuller LH, et al: Insulin-like growth factor-I and insulin are associated with the presence and advancement of adenomatous polyps. Gastroenterology 129:464-475, 2005 (Pubitemid 41096634)
28. Paley PJ: Angiogenesis in ovarian cancer: Molecular pathology and therapeutic strategies. Curr Oncol Rep 4:165-174, 2002
29. Yokoyama Y, Dhanabal M, Griffioen AW, et al: Synergy between angiostatin and endostatin: Inhibition of ovarian cancer growth. Cancer Res 60:2190-2196, 2000 (Pubitemid 30225182)
30. Bast RC Jr, Badgwell D, Lu Z, et al: New tumor markers: CA125 and beyond. Int J Gynecol Cancer 15:274-281, 2005 (suppl 3) (Pubitemid 43096594)
31. Bast RC Jr, Klug TL, St John E, et al: A radioimmunoassay using a monoclonal antibody to monitor the course of epithelial ovarian cancer. N Engl J Med 309:883-887, 1983 (Pubitemid 13014028)
32. Jacobs IJ, Rivera H, Oram DH, et al: Differential diagnosis of ovarian cancer with tumour markers CA 125, CA 15-3 and TAG 72.3. Br J Obstet Gynaecol 100:1120-1124, 1993 (Pubitemid 24003623)
33. Scambia G, Benedetti Panici P, Baiocchi G, et al: CA 15-3 as a tumor marker in gynecological malignancies. Gynecol Oncol 30:265-273, 1988
34. Buamah PK, Rake MO, Drake SR, et al: Serum CA 12-5 concentrations and CA 12-5/CEA ratios in patients with epithelial ovarian cancer. J Surg Oncol 44:97-99, 1990 (Pubitemid 20200305)
35. de Bruijn HW, ten Hoor KA, Boonstra H, et al: Cancer-associated antigen CA 195 in patients with mucinous ovarian tumours: A comparative analysis with CEA, TATI and CA 125 in serum specimens and cyst fluids. Tumour Biol 14:105-115, 1993
36. Yabushita H, Masuda T, Ogawa A, et al: Combination assay of CA125, TPA, IAP, CEA, and ferritin in serum for ovarian cancer. Gynecol Oncol 29:66-75, 1988
37. Gadducci A, Cosio S, Carpi A, et al: Serum tumor markers in the management of ovarian, endometrial and cervical cancer. Biomed Pharmacother 58:24-38, 2004 (Pubitemid 38117046)
38. Guadagni F, Roselli M, Cosimelli M, et al: CA 72-4 serum marker: A new tool in the management of carcinoma patients. Cancer Invest 13:227-238, 1995
39. Seppälä M, Pihko H, Ruoslahti E: Carcinoembryonic antigen and alpha fetoprotein in malignant tumors of the female genital tract. Cancer 35:1377-1381, 1975
40. Yamada T, Ikeda A, Okamoto Y, et al: High serum SCC antigen levels in two patients with ovarian cancer. Acta Obstet Gynecol Scand 76:283-285, 1997 (Pubitemid 27122540)
41. Gadducci A, Ferdeghini M, Cosio S, et al: The clinical relevance of serum CYFRA 21-1 assay in patients with ovarian cancer. Int J Gynecol Cancer 11:277-282, 2001 (Pubitemid 32751395)
42. Ouellet V, Le Page C, Madore J, et al: An apoptotic molecular network identified by microarray: On the TRAIL to new insights in epithelial ovarian cancer. Cancer 110:297-308, 2007 (Pubitemid 47121889)
43. Arts HJ, de Jong S, Hollema H, et al: Fas and Fas ligand in cyst fluids, serum and tumors of patients with benign and (borderline) malignant ovarian tumors. Int J Oncol 26:379-384, 2005
44. Paliouras M, Borgono C, Diamandis EP: Human tissue kallikreins: The cancer biomarker family. Cancer Lett 249:61-79, 2007 (Pubitemid 46427999)
45. Clements JA, Willemsen NM, Myers SA, et al: The tissue kallikrein family of serine proteases: Functional roles in human disease and potential as clinical biomarkers. Crit Rev Clin Lab Sci 41:265-312, 2004 (Pubitemid 38888061)
46. Acar A, Onan A, Coskun U, et al: Clinical significance of serum MMP-2 and MMP-7 in patients with ovarian cancer. Med Oncol 25:279-283, 2008
47. Dolo V, D'Ascenzo S, Violini S, et al: Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 17:131-140, 1999 (Pubitemid 29335439)
48. Rauvala M, Puistola U, Turpeenniemi-Hujanen T: Gelatinases and their tissue inhibitors in ovarian tumors; TIMP-1 is a predictive as well as a prognostic factor. Gynecol Oncol 99:656-663, 2005
49. Banks RE, Gearing AJ, Hemingway IK, et al: Circulating intercellular adhesion molecule-1 (ICAM-1), E-selectin and vascular cell adhesion molecule-1 (VCAM-1) in human malignancies. Br J Cancer 68:122-124, 1993 (Pubitemid 23178563)
50. Helzlsouer KJ, Alberg AJ, Gordon GB, et al: Serum gonadotropins and steroid hormones and the development of ovarian cancer. JAMA 274:1926-1930, 1995
51. Ylikorkala O, Kauppila A, Rajala T: Pituitary gonadotrophins and prolactin in patients with endometrial cancer, fibroids or ovarian tumours. Br J Obstet Gynaecol 86:901-904, 1979 (Pubitemid 10231432)
52. Ind T, Iles R, Shepherd J, et al: Serum concentrations of cancer antigen 125, placental alkaline phosphatase, cancer-associated serum antigen and free beta human chorionic gonadotrophin as prognostic markers for epithelial ovarian cancer. Br J Obstet Gynaecol 104:1024-1029, 1997 (Pubitemid 27400183)
53. Okamoto T, Niu R, Matsuo K, et al: Human chorionic gonadotropin beta-core fragment is directly produced by cancer cells. Life Sci 68:861-872, 2001 (Pubitemid 32168062)
54. Erturk E, Tuncel E: Polycystic ovarian disease and serum leptin levels? Fertil Steril 80:1068-1069, 2003
55. Sieminska L, Marek B, Kos-Kudla B, et al: Serum adiponectin in women with polycystic ovarian syndrome and its relation to clinical, metabolic and endocrine parameters. J Endocrinol Invest 27:528-534, 2004
56. Mor G, Visintin I, Lai Y, et al: Serum protein markers for early detection of ovarian cancer. Proc Natl Acad Sci U S A 102:7677-7682, 2005
57. Seow KM, Juan CC, Hsu YP, et al: Serum and follicular resistin levels in women with polycystic ovarian syndrome during IVF-stimulated cycles. Hum Reprod 20:117-121, 2005
58. Huang CY, Cheng WF, Lee CN, et al: Serum mesothelin in epithelial ovarian carcinoma: A new screening marker and prognostic factor. Anticancer Res 26:4721-4728, 2006
59. Hellström I, Raycraft J, Hayden-Ledbetter M, et al: The HE4 (WFDC2) protein is a biomarker for ovarian carcinoma. Cancer Res 63:3695-3700, 2003 (Pubitemid 36793054)
60. Abendstein B, Daxenbichler G, Windbichler G, et al: Predictive value of uPA, PAI-1, HER-2 and VEGF in the serum of ovarian cancer patients. Anticancer Res 20:569-572, 2000 (Pubitemid 30189723)
61. Koziol-Montewka M, Magrys A, Paluch-Oles J, et al: MPO and cytokines in the serum of cancer patients in the context of Candida colonization and infection. Immunol Invest 35:167-179, 2006
62. Gadomska H, Grzechocinska B, Janecki J, et al: Serum lipids concentration in women with benign and malignant ovarian tumours. Eur J Obstet Gynecol Reprod Biol 120:87-90, 2005 (Pubitemid 40615078)
63. Moore LE, Fung ET, McGuire M, et al: Evaluation of apolipoprotein A1 and posttranslationally modified forms of transthyretin as biomarkers for ovarian cancer detection in an independent study population. Cancer Epidemiol Biomarkers Prev 15:1641-1646, 2006 (Pubitemid 44497099)
64. Yam D, Ben-Hur H, Fink A, et al: Insulin and glucose status, tissue and plasma lipids in patients with tumours of the ovary or endometrium: Possible dietary implications. Br J Cancer 70:1186-1187, 1994 (Pubitemid 24358960)
65. Holen I, Shipman CM: Role of osteoprotegerin (OPG) in cancer. Clin Sci (Lond) 110:279-291, 2006 (Pubitemid 43348393)
66. Pietschmann P, Zielinski C, Woloszczuk W: Serum osteocalcin levels in breast cancer patients. J Cancer Res Clin Oncol 115:456-458, 1989 (Pubitemid 19246612)
67. Gu Y, Zeleniuch-Jacquotte A, Linkov F, et al: Reproducibility of serum cytokines and growth factors. Cytokine 45:44-49, 2009
68. Arslan AA, Gu Y, Zeleniuch-Jacquotte A, et al: Reproducibility of serum pituitary hormones in women. Cancer Epidemiol Biomarkers Prev 17:1880-1883, 2008
69. Linkov F, Gu Y, Arslan AA, et al: Reliability of tumor markers, chemokines, and metastasis-related molecules in serum. Eur Cytokine Netw 20:21-26, 2009
70. University of Pittsburgh Cancer Institute: Overview. http://www.upci. upmc.edu/facilities/luminex/index.html
71. Metropolis N, Rosenbluth AW, Rosenbluth MN, et al: Equation of state calculations by fast computing machines. J Chem Phys 21:1087, 1953
72. Robert CP, Casella G: Monte Carlo Statistical Methods. New York, NY, Springer Verlag, 2004
73. Fishman GS: Monte Carlo: Concepts, Algorithms, and Applications. New York, NY, Springer Verlag, 1995
74. Kucera E, Kainz C, Tempfer C, et al: Prostate specific antigen (PSA) in breast and ovarian cancer. Anticancer Res 17:4735-4737, 1997 (Pubitemid 28081774)
75. Callet N, Delaunay J, Pichon MF: Serum sICAM-1 (soluble intercellular adhesion molecule-1) and M-CSF (macrophage colony-stimulating growth factor) throughout monitoring of 34 non-serous ovarian cancers. Eur J Gynaecol Oncol 21:135-140, 2000 (Pubitemid 30240596)
76. Thierry van Dessel HJ, Lee PD, Faessen G, et al: Elevated serum levels of free insulin-like growth factor I in polycystic ovary syndrome. J Clin Endocrinol Metab 84:3030-3035, 1999 (Pubitemid 30646918)
77. Fahlbusch B, Metzner G, Schumann I, et al: Inhibition of macrophage migration by a factor from ascites fluids of ovarian cancer patients: II. Production and characterization of an anti-MIF antibody. Biomed Biochim Acta 45:371-384, 1986
78. Schummer M, Ng WV, Bumgarner RE, et al: Comparative hybridization of an array of 21,500 ovarian cDNAs for the discovery of genes overexpressed in ovarian carcinomas. Gene 238:375-385, 1999 (Pubitemid 29446174)
79. Borgoño CA, Fracchioli S, Yousef GM, et al: Favorable prognostic value of tissue human kallikrein 11 (hK11) in patients with ovarian carcinoma. Int J Cancer 106:605-610, 2003 (Pubitemid 36966221)
80. Diamandis EP, Scorilas A, Fracchioli S, et al: Human kallikrein 6 (hK6): A new potential serum biomarker for diagnosis and prognosis of ovarian carcinoma. J Clin Oncol 21:1035-1043, 2003 (Pubitemid 46594132)
81. Kim H, Scorilas A, Katsaros D, et al: Human kallikrein gene 5 (KLK5) expression is an indicator of poor prognosis in ovarian cancer. Br J Cancer 84:643-650, 2001 (Pubitemid 32238998)
82. Kishi T, Grass L, Soosaipillai A, et al: Human kallikrein 8, a novel biomarker for ovarian carcinoma. Cancer Res 63:2771-2774, 2003 (Pubitemid 36667147)
83. Kyriakopoulou LG, Yousef GM, Scorilas A, et al: Prognostic value of quantitatively assessed KLK7 expression in ovarian cancer. Clin Biochem 36:135-143, 2003 (Pubitemid 36287493)
84. Obiezu CV, Scorilas A, Katsaros D, et al: Higher human kallikrein gene 4 (KLK4) expression indicates poor prognosis of ovarian cancer patients. Clin Cancer Res 7:2380-2386, 2001 (Pubitemid 32751639)
85. Yousef GM, Diamandis EP: Expanded human tissue kallikrein family: A novel panel of cancer biomarkers. Tumour Biol 23:185-192, 2002 (Pubitemid 44858310)
86. Tempfer C, Zeisler H, Sliutz G, et al: Serum evaluation of interleukin 6 in ovarian cancer patients. Gynecol Oncol 66:27-30, 1997 (Pubitemid 27329303)
87. Macciò A, Lai P, Santona MC, et al: High serum levels of soluble IL-2 receptor, cytokines, and C reactive protein correlate with impairment of T cell response in patients with advanced epithelial ovarian cancer. Gynecol Oncol 69:248-252, 1998 (Pubitemid 28289968)
88. Bonfrer JM, Baan AW, Jansen E, et al: Technical evaluation of three second generation CA 125 assays. Eur J Clin Chem Clin Biochem 32:201-207, 1994 (Pubitemid 24096846)
89. McIntosh MW, Drescher C, Karlan B, et al: Combining CA 125 and SMR serum markers for diagnosis and early detection of ovarian carcinoma. Gynecol Oncol 95:9-15, 2004 (Pubitemid 39286271)
90. Nolen B, Marrangoni A, Velikokhatnaya L, et al: A serum based analysis of ovarian epithelial tumorigenesis. Gynecol Oncol 112:47-54, 2009
91. Lataifeh I, Marsden DE, Robertson G, et al: Presenting symptoms of epithelial ovarian cancer. Aust N Z J Obstet Gynaecol 45:211-214, 2005 (Pubitemid 40846934)
92. Westhoff C, Clark CJ: Benign ovarian cysts in England and Wales and in the United States. Br J Obstet Gynaecol 99:329-332, 1992
93. Jacobs IJ, Skates SJ, MacDonald N, et al: Screening for ovarian cancer: A pilot randomised controlled trial. Lancet 353:1207-1210, 1999 (Pubitemid 29168457)
94. Jemal A, Siegel R, Ward E, et al: Cancer statistics, 2008. CA Cancer J Clin 58:71-96, 2008
95. Skates SP, Pauler DK, Jacobs IJ: Screening based on the risk of cancer calculation from Bayesian hierarchical change-point and mixture models of longitudinal markers. J Am Stat Assoc 96:429-439, 2001
96. Menon U, Skates SJ, Lewis S, et al: Prospective study using the risk of ovarian cancer algorithm to screen for ovarian cancer. J Clin Oncol 23:7919-7926, 2005 (Pubitemid 46657391)