Effect of neoadjuvant chemoradiation on tumor-infiltrating/associated lymphocytes in locally advanced rectal cancers

Anticancer Research

Volumn 34, Issue 11, 2014, Pages 6505-6513

  Lim, Stephanie Hui Su ^a,b,c   Chua, Wei ^a,b   Cheng, Christina ^d   Descallar, Joseph ^b,c   Ng, Weng ^a,b   Solomon, Michael ^e,f,g   Bokey, Les ^a,b,d   Wong, Karen ^a,b,c   Lee, Mark T ^a,c   De Souza, Paul ^a,b,c,d   Shin, Joo Shik ^a,b,d   Lee, Cheok Soon ^a,b,c,d,f  

^a LIVERPOOL HOSPITAL   (Australia)

^b INGHAM INSTITUTE FOR APPLIED MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF WESTERN SYDNEY   (Australia)

^e ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^f UNIVERSITY OF SYDNEY   (Australia)

^g Surgical Outcomes Research Centre   (Australia)

Author keywords

CD3 CD4 CD8 lymphocytes; Colorectal cancer; NK cells; Radiation; Tumour microenvironment

Indexed keywords

ANTINEOPLASTIC AGENT; CD56 ANTIGEN; CD57 ANTIGEN; ANTINEOPLASTIC ANTIMETABOLITE; FLUOROURACIL;

ADJUVANT CHEMORADIOTHERAPY; ADULT; ADVANCED CANCER; ARTICLE; CANCER SURVIVAL; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLONOSCOPY; DISEASE FREE SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; RECTUM BIOPSY; RECTUM CANCER; RECTUM RESECTION; T LYMPHOCYTE; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR REGRESSION; ADJUVANT THERAPY; CANCER STAGING; CASE CONTROL STUDY; CHEMORADIOTHERAPY; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECTS; FOLLOW UP; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; RADIATION RESPONSE; RANDOMIZED CONTROLLED TRIAL; RECTAL NEOPLASMS; RETROSPECTIVE STUDY; SURVIVAL RATE; T LYMPHOCYTE SUBPOPULATION;

ANTIMETABOLITES, ANTINEOPLASTIC; CASE-CONTROL STUDIES; CHEMORADIOTHERAPY; FEMALE; FLUOROURACIL; FOLLOW-UP STUDIES; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; NEOADJUVANT THERAPY; NEOPLASM STAGING; PROGNOSIS; RECTAL NEOPLASMS; RETROSPECTIVE STUDIES; SURVIVAL RATE; T-LYMPHOCYTE SUBSETS; TISSUE ARRAY ANALYSIS;

EID: 84916215707     PISSN: 02507005     EISSN: 17917530     Source Type: Journal    
DOI: None     Document Type: Article

References (32)

1. Banner, BF, Savas L, Baker S and Woda BA: Characterization of the inflammatory cell populations in normal colon and colonic carcinomas. Virchows Arch B Cell Pathol Incl Mol Pathol 64(4): 213-220, 1993.
2. Hanahan, D and Weinberg RA: Hallmarks of cancer: the next generation. Cell 144(5): 646-674, 2011.
3. Wu, J and Lanier LL: Natural killer cells and cancer. Adv Cancer Res 90: 127-156, 2003.
4. Nosho, K, Baba Y, Tanaka N, Shima K, Hayashi M, Meyerhardt JA, Giovannucci E, Dranoff G, Fuchs CS, and Ogino S: Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol 222(4): 350-366, 2010.
5. Huh, JW, Lee JH and Kim HR: Prognostic significance of tumor-infiltrating lymphocytes for patients with colorectal cancer. Arch Surg 147(4): 366-372, 2012.
6. Ogino, S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, Glickman JN, Ferrone CR, Mino-Kenudson M, Tanaka N, Dranoff G, Giovannucci EL and Fuchs CS: Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 15(20): 6412-6420, 2009.
7. Baxevanis, CN, Papamichail M and Perez SA: Immune classification of colorectal cancer patients: impressive but how complete? Expert Opin Biol Ther 13(4): 517-526, 2013.
8. Tosolini, M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pages F and Galon J: Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res 71(4): 1263-1271, 2011.
9. Galon, J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH and Pages F: Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313(5795): 1960-1964, 2006.
10. Chaput, N, Svrcek M, Auperin A, Locher C, Drusch F, Malka D, Taieb J, Goere D, Ducreux M and Boige V: Tumour-infiltrating CD68+ and CD57+ cells predict patient outcome in stage II-III colorectal cancer. Br J Cancer 109(4): 1013-1022, 2013.
11. Yasuda, K, Nirei T, Sunami E, Nagawa H, and Kitayama J: Density of CD4(+) and CD8(+) T lymphocytes in biopsy samples can be a predictor of pathological response to chemoradiotherapy (CRT) for rectal cancer. Radiat Oncol 6: 49, 2011.
12. Anitei, MG, Zeitoun G, Mlecnik B, Marliot F, Haicheur N, Todosi AM, Kirilovsky A, Lagorce C, Bindea G, Ferariu D, Danciu M, Bruneval P, Scripcariu V, Chevallier JM, Zinzindohoue F, Berger A, Galon J and Pages F: Prognostic and predictive values of the immunoscore in patients with rectal cancer. Clin Cancer Res 20(7): 1891-1899, 2014.
13. Koda, K, Saito N, Oda K, Seike K, Kondo E, Ishizuka M, Takiguchi N and Miyazaki M: Natural killer cell activity and distant metastasis in rectal cancers treated surgically with and without neoadjuvant chemoradiotherapy. J Am Coll Surg 197(2): 254-260, 2003.
14. Zhang, Z, Su T, He L, Wang H, Ji G, Liu X, Zhang Y and Dong G: Identification and functional analysis of ligands for natural killer cell activating receptors in colon carcinoma. Tohoku J Exp Med 226(1): 59-68, 2012.
15. Bouzourene, H, Bosman FT, Seelentag W, Matter M and Coucke P: Importance of tumor regression assessment in predicting the outcome in patients with locally advanced rectal carcinoma who are treated with preoperative radiotherapy. Cancer 94(4): 1121-1130, 2002.
16. Coca, S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C, Martos JA and Moreno M: The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 79(12): 2320-2328, 1997.
17. Villegas, FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J, Zuil M and Callol L: Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35(1): 23-28, 2002.
18. Ishigami, S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H, Aridome K, Hokita S and Aikou T: Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88(3): 577-583, 2000.
19. Halama, N, Braun M, Kahlert C, Spille A, Quack C, Rahbari N, Koch M, Weitz J, Kloor M, Zoernig I, Schirmacher P, Brand K, Grabe N and Falk CS: Natural killer cells are scarce in colorectal carcinoma tissue despite high levels of chemokines and cytokines. Clin Cancer Res 17(4): 678-689, 2011.
20. Imai, K, Matsuyama S, Miyake S, Suga K and Nakachi K: Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356(9244): 1795-1799, 2000.
21. Galon, J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C, Nagtegaal ID, Palmqvist R, Masucci GV, Botti G, Tatangelo F, Delrio P, Maio M, Laghi L, Grizzi F, Asslaber M, D'Arrigo C, Vidal-Vanaclocha F, Zavadova E, Chouchane L, Ohashi PS, Hafezi-Bakhtiari S, Wouters BG, Roehrl M, Nguyen L, Kawakami Y, Hazama S, Okuno K, Ogino S, Gibbs P, Waring P, Sato N, Torigoe T, Itoh K, Patel PS, Shukla SN, Wang Y, Kopetz S, Sinicrope FA, Scripcariu V, Ascierto PA, Marincola FM, Fox BA and Pages F: Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. J Pathol 232(2): 199-209, 2014.
22. Galon, J, Pages F, Marincola FM, Angell HK, Thurin M, Lugli A, Zlobec I, Berger A, Bifulco C, Botti G, Tatangelo F, Britten CM, Kreiter S, Chouchane L, Delrio P, Arndt H, Asslaber M, Maio M, Masucci GV, Mihm M, Vidal-Vanaclocha F, Allison JP, Gnjatic S, Hakansson L, Huber C, Singh-Jasuja H, Ottensmeier C, Zwierzina H, Laghi L, Grizzi F, Ohashi PS, Shaw PA, Clarke BA, Wouters BG, Kawakami Y, Hazama S, Okuno K, Wang E, O'Donnell-Tormey J, Lagorce C, Pawelec G, Nishimura MI, Hawkins R, Lapointe R, Lundqvist A, Khleif SN, Ogino S, Gibbs P, Waring P, Sato N, Torigoe T, Itoh K, Patel PS, Shukla SN, Palmqvist R, Nagtegaal ID, Wang Y, D'Arrigo C, Kopetz S, Sinicrope FA, Trinchieri G, Gajewski TF, Ascierto PA and Fox BA: Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 10: 205, 2012.
23. Kitayama, J, Yasuda K, Kawai K, Sunami E and Nagawa H: Circulating lymphocyte is an important determinant of the effectiveness of preoperative radiotherapy in advanced rectal cancer. BMC Cancer 11: 64, 2011.
24. Halama, N, Michel S, Kloor M, Zoernig I, Pommerencke T, Doeberitz MVK, Schirmacher P, Weitz J, Grabe N and Jager D: The localization and density of immune cells in primary tumors of human metastatic colorectal cancer shows an association with response to chemotherapy. Cancer Immunity 9(A1): 2009.
25. Correale, P, Rotundo MS, Del Vecchio MT, Remondo C, Migali C, Ginanneschi C, Tsang KY, Licchetta A, Mannucci S, Loiacono L, Tassone P, Francini G and Tagliaferri P: Regulatory (FoxP3+) T-cell tumor infiltration is a favorable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy. Journal of Immunotherapy 33(4): 435-441, 2010.
26. Stone, HB, Peters LJ and Milas L: Effect of host immune capability on radiocurability and subsequent transplantability of a murine fibrosarcoma. Journal of the National Cancer Institute 63(5): 1229-1235, 1979.
27. Bosset, JF, Calais G, Mineur L, Maingon P, Radosevic-Jelic L, Daban A, Bardet E, Beny A, Briffaux A and Collette L: Enhanced tumorocidal effect of chemotherapy with preoperative radiotherapy for rectal cancer: preliminary results - EORTC 22921. J Clin Oncol 23(24): 5620-5627, 2005.
28. Demaria, S and Formenti SC: Role of T lymphocytes in tumor response to radiotherapy. Front Oncol 2: 95, 2012.
29. Li, YF, Yang ZB, Li Q, Li M and Xia CF: Influence of preoperative chemoradiotherapy, preoperative chemotherapy, and operation on immunity function in middle or lower rectal cancer patients. Zhonghua Yi Xue Za Zhi 88(37): 2629-2632, 2008.
30. Wichmann, MW, Meyer G, Adam M, Hochtlen-Vollmar W, Angele MK, Schalhorn A, Wilkowski R, Muller C and Schildberg FW: Detrimental immunologic effects of preoperative chemoradiotherapy in advanced rectal cancer. Dis Colon Rectum 46(7): 875-887, 2003.
31. Menon, AG, Janssen-van Rhijn CM, Morreau H, Putter H, Tollenaar RA, van de Velde CJ, Fleuren GJ and Kuppen PJ: Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest 84(4): 493-501, 2004.
32. Perez, RO, Habr-Gama A, dos Santos RM, Proscurshim I, Campos FG, Rawet V, Kiss D and Cecconello I: Peritumoral inflammatory infiltrate is not a prognostic factor in distal rectal cancer following neoadjuvant chemoradiation therapy. J Gastrointest Surg 11(11): 1534-1540, 2007.