Blood eosinophilic relative count is prognostic for breast cancer and associated with the presence of tumor at diagnosis and at time of relapse

References

• Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–11. doi:10.3322/caac.21492.
   PubMed Web of Science ®Google Scholar
• Denkert C, Loibl S, Noske A, Roller M, Müller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28(1):105–113. doi:10.1200/JCO.2009.23.7370.
   PubMed Web of Science ®Google Scholar
• Dieci MV, Criscitiello C, Goubar A, Viale G, Conte P, Guarneri V, Ficarra G, Mathieu MC, Delaloge S, Curigliano G, et al. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Ann Oncol. 2014;25(3):611–618. doi:10.1093/annonc/mdt556.
   PubMed Web of Science ®Google Scholar
• Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, Hirata T, Yonemori K, Ando M, Tamura K, Katsumata N. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat. 2012;132(3):793–805. doi:10.1007/s10549-011-1554-7.
   PubMed Web of Science ®Google Scholar
• Peng GL, Li L, Guo YW, Yu P, Yin XJ, Wang S, Liu CP. CD8(+) cytotoxic and FoxP3(+) regulatory T lymphocytes serve as prognostic factors in breast cancer. Am J Transl Res. 2019;11(8):5039–5053.
   PubMed Web of Science ®Google Scholar
• Ladoire S, Arnould L, Apetoh L, Coudert B, Martin F, Chauffert B, Fumoleau P, Ghiringhelli F. Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clin Cancer Res. 2008;14(8):2413–2420. doi:10.1158/1078-0432.CCR-07-4491.
   PubMed Web of Science ®Google Scholar
• Liu F, Lang R, Zhao J, Zhang X, Pringle GA, Fan Y, Yin D, Gu F, Yao Z, Fu L, et al. CD8⁺ cytotoxic T cell and FOXP3⁺ regulatory T cell infiltration in relation to breast cancer survival and molecular subtypes. Breast Cancer Res Treat. 2011;130(2):645–655. doi:10.1007/s10549-011-1647-3.
   PubMed Web of Science ®Google Scholar
• Gündüz S, Göksu SS, Arslan D, Tatli AM, Uysal M, Gündüz UR, Sevinç MM, Coşkun HS, Bozcuk H, Mutlu H, Savas B. Factors affecting disease-free survival in patients with human epidermal growth factor receptor 2-positive breast cancer who receive adjuvant trastuzumab. Mol Clin Oncol. 2015;3(5):1109–1112. doi:10.3892/mco.2015.610.
   PubMed Web of Science ®Google Scholar
• Ownby HE, Roi LD, Isenberg RR, Brennan MJ. Peripheral lymphocyte and eosinophil counts as indicators of prognosis in primary breast cancer. Cancer. 1983;52(1):126–130. doi:10.1002/1097-0142(19830701)52:1<126::AID-CNCR2820520123>3.0.CO;2-Y.
   PubMed Web of Science ®Google Scholar
• Papatestas AE, Lesnick GJ, Genkins G, Aufses AH Jr. The prognostic significance of peripheral lymphocyte counts in patients with breast carcinoma. Cancer. 1976;37(1):164–168. doi:10.1002/1097-0142(197601)37:1<164::AID-CNCR2820370123>3.0.CO;2-H.
   PubMed Web of Science ®Google Scholar
• Vicente Conesa MA, Garcia-Martinez E, Gonzalez Billalabeitia E, Chaves Benito A, Garcia Garcia T, Vicente Garcia V, Ayala de la Peña F. Predictive value of peripheral blood lymphocyte count in breast cancer patients treated with primary chemotherapy. Breast. 2012;21(4):468–474. doi:10.1016/j.breast.2011.11.002.
   PubMed Web of Science ®Google Scholar
• Pattison CW, Woods KL, Morrison JM. Lymphocytopenia as an independent predictor of early recurrence in breast cancer. Br J Cancer. 1987;55(1):75–76. doi:10.1038/bjc.1987.15.
   PubMed Web of Science ®Google Scholar
• Koh CH, Bhoo-Pathy N, Ng KL, Jabir RS, Tan GH, See MH, Jamaris S, Taib NA. Utility of pre-treatment neutrophil-lymphocyte ratio and platelet-lymphocyte ratio as prognostic factors in breast cancer. Br J Cancer. 2015;113(1):150–158. doi:10.1038/bjc.2015.183.
   PubMed Web of Science ®Google Scholar
• Zenan H, Zixiong L, Zhicheng Y, Mei H, Xiongbin Y, Tiantian W, Min D, Renbin L, Changchang J. Clinical prognostic evaluation of immunocytes in different molecular subtypes of breast cancer. J Cell Physiol. 2019;234(11):20584–20602. doi:10.1002/jcp.28662.
   PubMed Web of Science ®Google Scholar
• Balatoni T, Ladányi A, Fröhlich G, Czirbesz K, Kovács P, Pánczél G, Bence E, Plótár V, Liszkay G. Biomarkers associated with clinical outcome of advanced melanoma patients treated with ipilimumab. Pathol Oncol Res. 2020;26(1):317–325. doi:10.1007/s12253-018-0466-9.
   PubMed Web of Science ®Google Scholar
• Bernard-Tessier A, Jeanville P, Champiat S, Lazarovici J, Voisin AL, Mateus C, Lambotte O, Annereau M, Michot J-M. Immune-related eosinophilia induced by anti-programmed death 1 or death-ligand 1 antibodies. Eur J Cancer. 2017;81:135–137. doi:10.1016/j.ejca.2017.05.017.
   PubMed Web of Science ®Google Scholar
• Delyon J, Mateus C, Lefeuvre D, Lanoy E, Zitvogel L, Chaput N, Roy S, Eggermont AMM, Routier E, Robert C, et al. Experience in daily practice with ipilimumab for the treatment of patients with metastatic melanoma: an early increase in lymphocyte and eosinophil counts is associated with improved survival. Ann Oncol. 2013;24(6):1697–1703. doi:10.1093/annonc/mdt027.
   PubMed Web of Science ®Google Scholar
• Ferrucci PF, Gandini S, Cocorocchio E, Pala L, Baldini F, Mosconi M, Cappellini GCA, Albertazzi E, Martinoli C. Baseline relative eosinophil count as a predictive biomarker for ipilimumab treatment in advanced melanoma. Oncotarget. 2017;8(45):79809–79815. doi:10.18632/oncotarget.19748.
   PubMedGoogle Scholar
• Martens A, Wistuba-Hamprecht K, Geukes Foppen M, Yuan J, Postow MA, Wong P, Romano E, Khammari A, Dreno B, Capone M, et al. Baseline peripheral blood biomarkers associated with clinical outcome of advanced melanoma patients treated with ipilimumab. Clin Cancer Res. 2016;22(12):2908–2918. doi:10.1158/1078-0432.CCR-15-2412.
   PubMed Web of Science ®Google Scholar
• Moreira A, Leisgang W, Schuler G, Heinzerling L. Eosinophilic count as a biomarker for prognosis of melanoma patients and its importance in the response to immunotherapy. Immunotherapy. 2017;9(2):115–121. doi:10.2217/imt-2016-0138.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Tanaka R, Maruyama H, Ishitsuka Y, Okiyama N, Watanabe R, Fujimoto M, Fujisawa Y. Correlation between blood cell count and outcome of melanoma patients treated with anti-PD-1 antibodies. Jpn J Clin Oncol. 2019;49(5):431–437. doi:10.1093/jjco/hyy201.
   PubMed Web of Science ®Google Scholar
• Rosner S, Kwong E, Shoushtari AN, Friedman CF, Betof AS, Brady MS, Coit DG, Callahan MK, Wolchok JD, Chapman PB, et al. Peripheral blood clinical laboratory variables associated with outcomes following combination nivolumab and ipilimumab immunotherapy in melanoma. Cancer Med. 2018;7(3):690–697. doi:10.1002/cam4.1356.
   PubMed Web of Science ®Google Scholar
• Sibille A, Henket M, Corhay JL, Louis R, Duysinx B. Clinical benefit to programmed death-1 inhibition for non-small-cell lung cancer is associated with higher blood eosinophil levels. Acta Oncol. 2020;59(3):257–259. doi:10.1080/0284186X.2019.1695063.
   PubMed Web of Science ®Google Scholar
• Soyano AE, Dholaria B, Marin-Acevedo JA, Diehl N, Hodge D, Luo Y, Manochakian R, Chumsri S, Adjei A, Knutson KL, et al. Peripheral blood biomarkers correlate with outcomes in advanced non-small cell lung Cancer patients treated with anti-PD-1 antibodies. J Immunother Cancer. 2018;6(1):129. doi:10.1186/s40425-018-0447-2.
   PubMedGoogle Scholar
• Weide B, Martens A, Hassel JC, Berking C, Postow MA, Bisschop K, Simeone E, Mangana J, Schilling B, Di Giacomo AM, et al. Baseline biomarkers for outcome of melanoma patients treated with pembrolizumab. Clin Cancer Res. 2016;22(22):5487–5496. doi:10.1158/1078-0432.CCR-16-0127.
   PubMed Web of Science ®Google Scholar
• Onesti CE, Josse C, Poncin A, Frères P, Poulet C, Bours V, Jerusalem G. Predictive and prognostic role of peripheral blood eosinophil count in triple-negative and hormone receptor-negative/HER2-positive breast cancer patients undergoing neoadjuvant treatment. Oncotarget. 2018;9(72):33719–33733. doi:10.18632/oncotarget.26120.
   PubMedGoogle Scholar
• Bellera CA, Penel N, Ouali M, Bonvalot S, Casali PG, Nielsen OS, Delannes M, Litière S, Bonnetain F, Dabakuyo TS, et al. Guidelines for time-to-event end point definitions in sarcomas and gastrointestinal stromal tumors (GIST) trials: results of the DATECAN initiative (Definition for the Assessment of Time-to-event Endpoints in CANcer trials). Ann Oncol. 2015;26(5):865–872. doi:10.1093/annonc/mdu360.
   PubMed Web of Science ®Google Scholar
• Gourgou-Bourgade S, Cameron D, Poortmans P, Asselain B, Azria D, Cardoso F, A’Hern R, Bliss J, Bogaerts J, Bonnefoi H, et al. Guidelines for time-to-event end point definitions in breast cancer trials: results of the DATECAN initiative (Definition for the Assessment of Time-to-event Endpoints in CANcer trials)†. Ann Oncol. 2015;26(5):873–879. doi:10.1093/annonc/mdv106.
   PubMed Web of Science ®Google Scholar
• Reichman H, Karo-Atar D, Munitz A. Emerging roles for eosinophils in the tumor microenvironment. Trends Cancer. 2016;2(11):664–675. doi:10.1016/j.trecan.2016.10.002.
   PubMed Web of Science ®Google Scholar
• Carretero R, Sektioglu IM, Garbi N, Salgado OC, Beckhove P, Hämmerling GJ. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat Immunol. 2015;16(6):609–617. doi:10.1038/ni.3159.
   PubMed Web of Science ®Google Scholar
• Mattes J, Hulett M, Xie W, Hogan S, Rothenberg ME, Foster P, Parish C. Immunotherapy of cytotoxic T cell-resistant tumors by T helper 2 cells: an eotaxin and STAT6-dependent process. J Exp Med. 2003;197(3):387–393. doi:10.1084/jem.20021683.
   PubMed Web of Science ®Google Scholar
• Gatault S, Legrand F, Delbeke M, Loiseau S, Capron M. Involvement of eosinophils in the anti-tumor response. Cancer Immunol Immunother. 2012;61(9):1527–1534. doi:10.1007/s00262-012-1288-3.
   PubMed Web of Science ®Google Scholar
• Jain M, Kasetty S, Sudheendra US, Tijare M, Khan S, Desai A. Assessment of tissue eosinophilia as a prognosticator in oral epithelial dysplasia and oral squamous cell carcinoma-an image analysis study. Patholog Res Int. 2014;2014:507512.
   PubMedGoogle Scholar
• De Paz D, Chang KP, Kao HK, Lao WW, Huang YC, Chang YL, Huang Y. Clinical implications of tumor-associated tissue eosinophilia in tongue squamous cell carcinoma. Laryngoscope. 2019;129(5):1123–1129. doi:10.1002/lary.27413.
   PubMed Web of Science ®Google Scholar
• Peurala E, Tuominen M, Löyttyniemi E, Syrjänen S, Rautava J. Eosinophilia is a favorable prognostic marker for oral cavity and lip squamous cell carcinoma. APMIS. 2018;126(3):201–207. doi:10.1111/apm.12809.
   PubMed Web of Science ®Google Scholar
• Samoszuk MK, Nguyen V, Gluzman I, Pham JH. Occult deposition of eosinophil peroxidase in a subset of human breast carcinomas. Am J Pathol. 1996;148:701–706.
   PubMed Web of Science ®Google Scholar
• Ali HR, Chlon L, Pharoah PD, Markowetz F, Caldas C, Ladanyi M. Patterns of immune infiltration in breast cancer and their clinical implications: a gene-expression-based retrospective study. PLoS Med. 2016;13(12):e1002194. doi:10.1371/journal.pmed.1002194.
   PubMed Web of Science ®Google Scholar
• Szalayova G, Ogrodnik A, Spencer B, Wade J, Bunn J, Ambaye A, James T, Rincon M. Human breast cancer biopsies induce eosinophil recruitment and enhance adjacent cancer cell proliferation. Breast Cancer Res Treat. 2016;157(3):461–474. doi:10.1007/s10549-016-3839-3.
   PubMed Web of Science ®Google Scholar
• Lucarini V, Ziccheddu G, Macchia I, La Sorsa V, Peschiaroli F, Buccione C, Sistigu A, Sanchez M, Andreone S, D’Urso MT. IL-33 restricts tumor growth and inhibits pulmonary metastasis in melanoma-bearing mice through eosinophils. Oncoimmunology. 2017;6(6):e1317420. doi:10.1080/2162402X.2017.1317420.
   PubMed Web of Science ®Google Scholar
• Qi L, Zhang Q, Miao Y, Kang W, Tian Z, Xu D, Xiao W, Fang F. Interleukin-33 activates and recruits natural killer cells to inhibit pulmonary metastatic cancer development. Int J Cancer. 2020;146(5):1421–1434. doi:10.1002/ijc.32779.
   PubMed Web of Science ®Google Scholar
• Jovanovic IP, Pejnovic NN, Radosavljevic GD, Pantic JM, Milovanovic MZ, Arsenijevic NN, Lukic ML. Interleukin-33/ST2 axis promotes breast cancer growth and metastases by facilitating intratumoral accumulation of immunosuppressive and innate lymphoid cells. Int J Cancer. 2014;134(7):1669–1682. doi:10.1002/ijc.28481.
   PubMed Web of Science ®Google Scholar
• Xiao P, Wan X, Cui B, Liu Y, Qiu C, Rong J, Zheng M, Song Y, Chen L, He J, et al. Interleukin 33 in tumor microenvironment is crucial for the accumulation and function of myeloid-derived suppressor cells. Oncoimmunology. 2016;5(1):e1063772. doi:10.1080/2162402X.2015.1063772.
   PubMed Web of Science ®Google Scholar
• Benatar T, Cao MY, Lee Y, Lightfoot J, Feng N, Gu X, Lee V, Jin H, Wang M, Wright JA, et al. IL-17E, a proinflammatory cytokine, has antitumor efficacy against several tumor types in vivo. Cancer Immunol Immunother. 2010;59(6):805–817. doi:10.1007/s00262-009-0802-8.
   PubMed Web of Science ®Google Scholar
• Zheng X, Zhang N, Qian L, Wang X, Fan P, Kuai J, Lin S, Liu C, Jiang W, Qin S, et al. CTLA4 blockade promotes vessel normalization in breast tumors via the accumulation of eosinophils. Int J Cancer. 2020;146(6):1730–1740. doi:10.1002/ijc.32829.
   PubMed Web of Science ®Google Scholar
• Nikolich-Žugich J. The twilight of immunity: emerging concepts in aging of the immune system. Nat Immunol. 2018;19(1):10–19. doi:10.1038/s41590-017-0006-x.
   PubMed Web of Science ®Google Scholar
• Wu L, Saxena S, Awaji M, Singh RK. Tumor-associated neutrophils in cancer: going pro. Cancers. 2019;11(4):4. doi:10.3390/cancers11040564.
   Web of Science ®Google Scholar