Dose-response association of CD8+ tumor-infiltrating lymphocytes and survival time in high-grade serous ovarian cancer

JAMA Oncology

Volumn 3, Issue 12, 2017, Pages

  Goode, Ellen L ^a   Block, Matthew S ^a   Kalli, Kimberly R ^a   Vierkant, Robert A ^a   Chen, Wenqian ^b   Fogarty, Zachary C ^a   Gentry Maharaj, Aleksandra ^c   Tołoczko, Aleksandra ^d   Hein, Alexander ^e   Bouligny, Aliecia L ^a,f   Jensen, Allan ^g   Osorio, Ana ^h,i   Hartkopf, Andreas D ^j   Ryan, Andy ^c   Chudecka Głaz, Anita ^d   Magliocco, Anthony M ^k   Hartmann, Arndt ^e   Jung, Audrey Y ^l   Gao, Bo ^m   Hernandez, Brenda Y ⁿ   Fridley, Brooke L ^k   McCauley, Bryan M ^a   Kennedy, Catherine J ^m,o   Wang, Chen ^a   Karpinskyj, Chloe ^c   de Sousa, Christiani B ^p   Tiezzi, Daniel G ^p   Wachter, David L ^e   Herpel, Esther ^q   Taran, Florin Andrei ^j   Modugno, Francesmary ^r,s,t   Nelson, Gregg ^u   Lubiński, Jan ^d   Menkiszak, Janusz ^d   Alsop, Jennifer ^v   Lester, Jenny ^w   Garcia Donas, Jesus ^x   Nation, Jill ^u   Hung, Jillian ^m,o   Palacios, Jose ^y   Rothstein, Joseph H ^z   Kelley, Joseph L ^r   de Andrade, Jurandyr M ^p   Robles Diaz, Luis ^aa   Intermaggio, Maria P ^ab   Widschwendter, Martin ^c   Beckmann, Matthias W ^e   Ruebner, Matthias ^e   Jimenez Linan, Mercedes ^ac   Singh, Naveena ^ad   Oszurek, Oleg ^d   Harnett, Paul R ^m   Rambau, Peter F ^b,ae   Sinn, Peter ^af   Wagner, Philipp ^j   Ghatage, Prafull ^u   Sharma, Raghwa ^m,ag   Edwards, Robert P ^r   Ness, Roberta B ^ah   Orsulic, Sandra ^w   Brucker, Sara Y ^j   Johnatty, Sharon E ^ai   Longacre, Teri A ^aj   Eilber, Ursula ^l   McGuire, Valerie ^aj   Sieh, Weiva ^z   Natanzon, Yanina ^a   Li, Zheng ^a,ak   Whittemore, Alice S ^aj   deFazio, Anna ^m,o   Staebler, Annette ^j   Karlan, Beth Y ^w   Gilks, Blake ^al   Bowtell, David D ^am,an,ao   Hogdall, Estrid ^g,ap   Candido dos Reis, Francisco J ^p   Steed, Helen ^aq   Campbell, Ian G ^am,an,ar   Gronwald, Jacek ^d   Benitez, Javier ^h,i   Koziak, Jennifer M ^as   Chang Claude, Jenny ^l,at   Moysich, Kirsten B ^au   Kelemen, Linda E ^av   Cook, Linda S ^aw   Goodman, Marc T ^w   Garcia, Maria Jose ^h,i   Fasching, Peter A ^e,ax   Kommoss, Stefan ^j   Deen, Suha ^ay   Kjaer, Susanne K ^g,ap   Menon, Usha ^c   Brenton, James D ^az,ba   Pharoah, Paul D P ^v,bb   Chenevix Trench, Georgia ^ai   Huntsman, David G ^bc,bd   Winham, Stacey J ^a   Kobel, Martin ^b   Ramus, Susan J ^ab,ao   more..

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d POMERANIAN MEDICAL UNIVERSITY   (Poland)

^e UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^f SPELMAN COLLEGE   (United States)

^g DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^h Structural Biology and Biocomputing Programme   (Spain)

ⁱ CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^j UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^k H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^l GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^m UNIVERSITY OF SYDNEY   (Australia)

ⁿ UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^o WESTMEAD HOSPITAL   (Australia)

^p UNIVERSITY OF SÃO PAULO   (Brazil)

^q UNIVERSITY OF HEIDELBERG   (Germany)

^r UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^s UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^t UNIVERSITY OF PITTSBURGH   (United States)

^u UNIVERSITY OF CALGARY   (Canada)

^v UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^w CEDARS SINAI MEDICAL CENTER   (United States)

^x Facultad HM Hospitales de Ciencias de la Salud de la UCJC   (Spain)

^y HOSPITAL RAMÓN Y CAJAL   (Spain)

^z MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^aa HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^ab UNIVERSITY OF NEW SOUTH WALES   (Australia)

^ac ADDENBROOKE S HOSPITAL   (United Kingdom)

^ad BARTS HEALTH NHS TRUST   (United Kingdom)

^ae CATHOLIC UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

^af UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^ag UNIVERSITY OF WESTERN SYDNEY   (Australia)

^ah UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^ai QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^aj STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^ak KUNMING MEDICAL UNIVERSITY   (China)

^al UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^am PETER MACCALLUM CANCER CENTRE   (Australia)

^an UNIVERSITY OF MELBOURNE   (Australia)

^ao GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^ap UNIVERSITY OF COPENHAGEN   (Denmark)

^aq ROYAL ALEXANDRA HOSPITAL   (Canada)

^ar UNIVERSITY OF MELBOURNE   (Australia)

^as ALBERTA HEALTH SERVICES   (Canada)

^at UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^au ROSWELL PARK CANCER INSTITUTE   (United States)

^av MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^aw UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^ax UNIVERSITY OF CALIFORNIA   (United States)

^ay QUEEN S MEDICAL CENTRE   (United Kingdom)

^az UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^ba Cambridge Experimental Cancer Medicine Centre   (United Kingdom)

^bb UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^bc UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^bd BRITISH COLUMBIA CANCER AGENCY   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BRCA2 PROTEIN; BRCA2 PROTEIN, HUMAN; CD8 ANTIGEN;

CANCER GRADING; CLINICAL TRIAL; COHORT ANALYSIS; CYSTADENOCARCINOMA; DRUG THERAPY; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; MUTATION; OVARY TUMOR; PATHOLOGY; PROSPECTIVE STUDY; SURVIVAL ANALYSIS; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE;

BRCA2 PROTEIN; CARCINOMA, OVARIAN EPITHELIAL; CD8 ANTIGENS; COHORT STUDIES; CYSTADENOCARCINOMA, SEROUS; FEMALE; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; MUTATION; NEOPLASM GRADING; OVARIAN NEOPLASMS; PROSPECTIVE STUDIES; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 85044128994     PISSN: 23742437     EISSN: 23742445     Source Type: Journal    
DOI: 10.1001/jamaoncol.2017.3290     Document Type: Article

References (54)

1. Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67(1):7-30.
2. Hamanishi J, Mandai M, Ikeda T, et al. Safety and antitumor activity of anti-PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol. 2015;33(34):4015-4022.
3. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366(26): 2455-2465.
4. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348 (3):203-213.
5. Tomsová M, Melichar B, Sedláková I, Steiner I. Prognostic significance of CD3+ tumor-infiltrating lymphocytes in ovarian carcinoma. Gynecol Oncol. 2008;108(2):415-420.
6. Han LY, Fletcher MS, Urbauer DL, et al. HLA class I antigen processing machinery component expression and intratumoral T-cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res. 2008;14(11):3372-3379.
7. Clarke B, Tinker AV, Lee CH, et al. Intraepithelial T cells and prognosis in ovarian carcinoma: novel associations with stage, tumor type, and BRCA1 loss. Mod Pathol. 2009;22(3):393-402.
8. Hwang WT, Adams SF, Tahirovic E, Hagemann IS, Coukos G. Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol Oncol. 2012;124(2):192-198.
9. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol. 2013;31: 443-473.
10. Sato E, Olson SH, Ahn J, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A. 2005;102(51):18538-18543.
11. Callahan MJ, Nagymanyoki Z, Bonome T, et al. Increased HLA-DMB expression in the tumor epithelium is associated with increased CTL infiltration and improved prognosis in advanced-stage serous ovarian cancer. Clin Cancer Res. 2008;14(23):7667-7673.
12. Preston CC, Maurer MJ, Oberg AL, et al. The ratios of CD8+ T cells to CD4+CD25+ FOXP3+ and FOXP3- T cells correlate with poor clinical outcome in human serous ovarian cancer. PLoS One. 2013;8 (11):e80063.
13. Kurman RJ. Origin and molecular pathogenesis of ovarian high-grade serous carcinoma. Ann Oncol. 2013;24(suppl 10):x16-x21.
14. Worley MJ, Welch WR, Berkowitz RS, Ng SW. Endometriosis-associated ovarian cancer: a review of pathogenesis. Int J Mol Sci. 2013;14(3):5367-5379.
15. Mabuchi S, Sugiyama T, Kimura T. Clear cell carcinoma of the ovary: molecular insights and future therapeutic perspectives. J Gynecol Oncol. 2016;27(3):e31.
16. Kelemen LE, Köbel M. Mucinous carcinomas of the ovary and colorectum: different organ, same dilemma. Lancet Oncol. 2011;12(11):1071-1080.
17. Emmanuel C, Chiew YE, George J, et al; Australian Ovarian Cancer Study (AOCS). Genomic classification of serous ovarian cancer with adjacent borderline differentiates RAS pathway and TP53-mutant tumors and identifies NRAS as an oncogenic driver. Clin Cancer Res. 2014;20(24): 6618-6630.
18. Oswald AJ, Gourley C. Low-grade epithelial ovarian cancer: a number of distinct clinical entities? Curr Opin Oncol. 2015;27(5):412-419.
19. Grabowski JP, Harter P, Heitz F, et al. Operability and chemotherapy responsiveness in advanced low-grade serous ovarian cancer: an analysis of the AGO Study Group metadatabase. Gynecol Oncol. 2016;140(3):457-462.
20. Fader AN, Java J, Ueda S, et al; Gynecologic Oncology Group (GOG). Survival in women with grade 1 serous ovarian carcinoma. Obstet Gynecol. 2013;122(2, pt 1):225-232.
21. Köbel M, Bak J, Bertelsen BI, et al. Ovarian carcinoma histotype determination is highly reproducible, and is improved through the use of immunohistochemistry. Histopathology. 2014;64 (7):1004-1013.
22. Ramalingam P. Morphologic, immunophenotypic, and molecular features of epithelial ovarian cancer. Oncology (Williston Park). 2016;30(2):166-176.
23. Köbel M, Kalloger SE, Boyd N, et al. Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med. 2008;5(12):e232.
24. Köbel M, Madore J, Ramus SJ, et al; AOCS Study Group. Evidence for a time-dependent association between FOLR1 expression and survival from ovarian carcinoma: implications for clinical testing: an Ovarian Tumour Tissue Analysis consortium study. Br J Cancer. 2014;111(12):2297-2307.
25. Köbel M, Kalloger SE, Lee S, et al; Ovarian Tumor Tissue Analysis consortium. Biomarker-based ovarian carcinoma typing: a histologic investigation in the ovarian tumor tissue analysis consortium. Cancer Epidemiol Biomarkers Prev. 2013;22(10):1677-1686.
26. Sieh W, Köbel M, Longacre TA, et al. Hormone-receptor expression and ovarian cancer survival: an Ovarian Tumor Tissue Analysis consortium study. Lancet Oncol. 2013;14(9):853-862.
27. Köbel M, Rahimi K, Rambau PF, et al. An immunohistochemical algorithm for ovarian carcinoma typing. Int J Gynecol Pathol. 2016;35(5): 430-441.
28. College of American Pathologists. Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. 2016; http://www.cap.org/ShowProperty?nodePath=/UCMCon/Contribution%20Folders/WebContent /pdf/cp-colon-16protocol-3400.pdf. Accessed August 22, 2017.
29. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM; Statistics Subcommittee of the NCI-EORTC Working Group on Cancer Diagnostics. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer. 2005;93(4):387-391.
30. Eilers PHC, Marx BD. Flexible smoothing with B-splines and penalties. Stat Sci. 1996;11(2):89-102.
31. Budczies J, Klauschen F, Sinn BV, et al. Cutoff Finder: a comprehensive and straightforward web application enabling rapid biomarker cutoff optimization. PLoS One. 2012;7(12):e51862.
32. Kar SP, Berchuck A, Gayther SA, et al. Common genetic variation and susceptibility to ovarian cancer: current insights and future directions [published online June 14, 2017]. Cancer Epidemiol Biomarkers Prev. 2017;cebp.0315.2017. doi:10.1158/1055-9965.EPI-17-0315
33. Candido-dos-Reis FJ, Song H, Goode EL, et al; for EMBRACE; kConFab Investigators; Australian Ovarian Cancer Study Group. Germline mutation in BRCA1 or BRCA2 and ten-year survival for women diagnosed with epithelial ovarian cancer. Clin Cancer Res. 2015;21(3):652-657.
34. Rambau PF, Duggan MA, Ghatage P, et al. Significant frequency of MSH2/MSH6 abnormality in ovarian endometrioid carcinoma supports histotype-specific Lynch syndrome screening in ovarian carcinomas. Histopathology. 2016;69(2): 288-297.
35. McMeekin DS, Tritchler DL, Cohn DE, et al. Clinicopathologic significance of mismatch repair defects in endometrial cancer: an NRG Oncology/Gynecologic Oncology Group study. J Clin Oncol. 2016;34(25):3062-3068.
36. Kandoth C, Schultz N, Cherniack AD, et al; Cancer Genome Atlas Research Network. Integrated genomic characterization of endometrial carcinoma. Nature. 2013;497(7447):67-73.
37. Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124-128.
38. McGranahan N, Furness AJ, Rosenthal R, et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016;351(6280):1463-1469.
39. Strickland KC, Howitt BE, Shukla SA, et al. Association and prognostic significance of BRCA1/2-mutation status with neoantigen load, number of tumor-infiltrating lymphocytes and expression of PD-1/PD-L1 in high grade serous ovarian cancer. Oncotarget. 2016;7(12):13587-13598.
40. Bolton KL, Chenevix-Trench G, Goh C, et al; EMBRACE; kConFab Investigators; Cancer Genome Atlas Research Network. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA. 2012; 307(4):382-390.
41. Sun C, Li N, Ding D, et al. The role of BRCA status on the prognosis of patients with epithelial ovarian cancer: a systematic review of the literature with a meta-analysis. PLoS One. 2014;9(5):e95285.
42. Galon J, Pagès F, Marincola FM, et al. Cancer classification using the Immunoscore: a worldwide task force. J Transl Med. 2012;10:205.
43. Denkert C, Wienert S, Poterie A, et al. Standardized evaluation of tumor-infiltrating lymphocytes in breast cancer: results of the ring studies of the international immuno-oncology biomarker working group. Mod Pathol. 2016;29 (10):1155-1164.
44. Hida AI, Ohi Y. Evaluation of tumor-infiltrating lymphocytes in breast cancer: proposal of a simpler method. Ann Oncol. 2015;26(11):2351.
45. Mesnage SJL, Auguste A, Genestie C, et al. Neoadjuvant chemotherapy (NACT) increases immune infiltration and programmed death-ligand 1 (PD-L1) expression in epithelial ovarian cancer (EOC). Ann Oncol. 2017;28(3):651-657.
46. Vergote I, Tropé CG, Amant F, et al; European Organization for Research and Treatment of Cancer-Gynaecological Cancer Group; NCIC Clinical Trials Group. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N Engl J Med. 2010;363(10):943-953.
47. Melamed A, Hinchcliff EM, Clemmer JT, et al. Trends in the use of neoadjuvant chemotherapy for advanced ovarian cancer in the United States. Gynecol Oncol. 2016;143(2):236-240.
48. Verhaak RG, Tamayo P, Yang JY, et al; Cancer Genome Atlas Research Network. Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J Clin Invest. 2013;123(1):517-525.
49. Tothill RW, Tinker AV, George J, et al; Australian Ovarian Cancer Study Group. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res. 2008;14(16):5198-5208.
50. Konecny GE, Wang C, Hamidi H, et al. Prognostic and therapeutic relevance of molecular subtypes in high-grade serous ovarian cancer. J Natl Cancer Inst. 2014;106(10):dju249.
51. Phelan CM, Kuchenbaecker KB, Tyrer JP, et al; AOCS study group; EMBRACE Study; GEMO Study Collaborators; HEBON Study; KConFab Investigators; OPAL study group. Identification of 12 new susceptibility loci for different histotypes of epithelial ovarian cancer. Nat Genet. 2017;49(5): 680-691.
52. Cannioto RA, Trabert B, Poole EM, Schildkraut JM. Ovarian cancer epidemiology in the era of collaborative team science. Cancer Causes Control. 2017;28(5):487-495.
53. Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures, cytolytic T-cell responses, and superior prognosis in ovarian cancer. Clin Cancer Res. 2016;22(12):3005-3015.
54. Loi S, Sirtaine N, Piette F, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol. 2013;31(7):860-867.