Prognostic role of pre-diagnostic circulating inflammatory biomarkers in breast cancer survival: evidence from the EPIC cohort study.
Journal
British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635
Informations de publication
Date de publication:
28 Sep 2024
28 Sep 2024
Historique:
received:
05
03
2024
accepted:
13
09
2024
revised:
09
09
2024
medline:
29
9
2024
pubmed:
29
9
2024
entrez:
28
9
2024
Statut:
aheadofprint
Résumé
Inflammation influences tumour progression and cancer prognosis, but its role preceding breast cancer (BC) and its prognostic implications remain inconclusive. We studied pre-diagnostic plasma inflammatory biomarkers in 1538 women with BC from the EPIC study. Cox proportional hazards models assessed their relationship with all-cause and BC-specific mortality, adjusting for tumour characteristics and lifestyle factors. Over a 7-year follow-up after diagnosis, 229 women died, 163 from BC. Elevated IL-6 levels were associated with increased all-cause mortality risk (HR Higher pre-diagnosis IL-6 levels suggest poorer long-term survival among BC survivors. In postmenopausal survivors, elevated IL-6, IL-10, and TNFα and inflammatory scores seem to predict all-cause mortality.
Sections du résumé
BACKGROUND
BACKGROUND
Inflammation influences tumour progression and cancer prognosis, but its role preceding breast cancer (BC) and its prognostic implications remain inconclusive.
METHODS
METHODS
We studied pre-diagnostic plasma inflammatory biomarkers in 1538 women with BC from the EPIC study. Cox proportional hazards models assessed their relationship with all-cause and BC-specific mortality, adjusting for tumour characteristics and lifestyle factors.
RESULTS
RESULTS
Over a 7-year follow-up after diagnosis, 229 women died, 163 from BC. Elevated IL-6 levels were associated with increased all-cause mortality risk (HR
CONCLUSIONS
CONCLUSIONS
Higher pre-diagnosis IL-6 levels suggest poorer long-term survival among BC survivors. In postmenopausal survivors, elevated IL-6, IL-10, and TNFα and inflammatory scores seem to predict all-cause mortality.
Identifiants
pubmed: 39342063
doi: 10.1038/s41416-024-02858-6
pii: 10.1038/s41416-024-02858-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : FI19/00197
Organisme : Fundación Científica Asociación Española Contra el Cáncer (Scientific Foundation, Spanish Association Against Cancer)
ID : PRYES211366AGUD
Informations de copyright
© 2024. The Author(s).
Références
Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global Cancer Observatory: Cancer today. International Agency for Research on Cancer. 2020. http://gco.iarc.fr/today . Accessed 13 Jun 2023.
Furman D, Campisi J, Verdin E, Carrera-Bastos P, Targ S, Franceschi C, et al. Chronic inflammation in the etiology of disease across the life span. Nat Med. 2019;25:1822–32.
doi: 10.1038/s41591-019-0675-0
pubmed: 31806905
pmcid: 7147972
Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
doi: 10.1016/j.cell.2011.02.013
pubmed: 21376230
Abubakar M, Zhang J, Ahearn TU, Koka H, Guo C, Lawrence SM, et al. Tumor-associated stromal cellular density as a predictor of recurrence and mortality in breast cancer: results from ethnically-diverse study populations. Cancer Epidemiol Biomark Prev. 2021;30:1397–407.
doi: 10.1158/1055-9965.EPI-21-0055
Allin KH, Nordestgaard BG, Flyger H, Bojesen SE. Elevated pre-treatment levels of plasma C-reactive protein are associated with poor prognosis after breast cancer: a cohort study. Breast Cancer Res. 2011;13:R55.
doi: 10.1186/bcr2891
pubmed: 21639875
pmcid: 3218944
Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, et al. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol. 2009;27:3437–44.
doi: 10.1200/JCO.2008.18.9068
pubmed: 19470939
pmcid: 2717751
Al Murri AM, Wilson C, Lannigan A, Doughty JC, Angerson WJ, McArdle CS, et al. Evaluation of the relationship between the systemic inflammatory response and cancer-specific survival in patients with primary operable breast cancer. Br J Cancer. 2007;96:891–5.
doi: 10.1038/sj.bjc.6603682
pubmed: 17375036
pmcid: 2360103
Pasanisi P, Venturelli E, Morelli D, Fontana L, Secreto G, Berrino F. Serum insulin-like growth factor-I and platelet-derived growth factor as biomarkers of breast cancer prognosis. Cancer Epidemiol Biomark Prev. 2008;17:1719–22.
doi: 10.1158/1055-9965.EPI-07-0654
Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5:1113–24.
doi: 10.1079/PHN2002394
pubmed: 12639222
Cairat M, Rinaldi S, Navionis AS, Romieu I, Biessy C, Viallon V, et al. Circulating inflammatory biomarkers, adipokines and breast cancer risk—a case-control study nested within the EPIC cohort. BMC Med. 2022;20:118.
doi: 10.1186/s12916-022-02319-y
pubmed: 35430795
pmcid: 9014562
Agudo A, Cayssials V, Bonet C, Tjønneland A, Overvad K, Boutron-Ruault MC, et al. Inflammatory potential of the diet and risk of gastric cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Am J Clin Nutr. 2018;107:607–16.
doi: 10.1093/ajcn/nqy002
pubmed: 29635497
Castro-Espin C, Agudo A, Bonet C, Katzke V, Turzanski-Fortner R, Aleksandrova K, et al. Inflammatory potential of the diet and risk of breast cancer in the European Investigation into Cancer and Nutrition (EPIC) study. Eur J Epidemiol. 2021;36:953–64.
doi: 10.1007/s10654-021-00772-2
pubmed: 34148186
Castro-Espin C, Bonet C, Crous-Bou M, Katzke V, Le Cornet C, Jannasch F, et al. Dietary patterns related to biological mechanisms and survival after breast cancer diagnosis: results from a cohort study. Br J Cancer. 2023;128:1301–10.
Fine JP, Gray RJ. A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc. 1999;94:496–509.
doi: 10.1080/01621459.1999.10474144
Guo Y, Xu F, Lu T, Duan Z, Zhang Z. Interleukin-6 signaling pathway in targeted therapy for cancer. Cancer Treat Rev. 2012;38:904–10.
doi: 10.1016/j.ctrv.2012.04.007
pubmed: 22651903
Esquivel-Velázquez M, Ostoa-Saloma P, Palacios-Arreola MI, Nava-Castro KE, Castro JI, Morales-Montor J. The role of cytokines in breast cancer development and progression. J Interferon Cytokine Res. 2015;35:1–16.
doi: 10.1089/jir.2014.0026
pubmed: 25068787
pmcid: 4291218
Lin S, Gan Z, Han K, Yao Y, Min D. Interleukin-6 as a prognostic marker for breast cancer: a meta-analysis. Tumori. 2015;101:535–41.
doi: 10.5301/tj.5000357
pubmed: 26045123
Tsoi H, Man EPS, Chau KM, Khoo US. Targeting the IL-6/STAT3 signalling cascade to reverse tamoxifen resistance in estrogen receptor positive breast cancer. Cancers. 2021;13:1511.
doi: 10.3390/cancers13071511
pubmed: 33806019
pmcid: 8036560
Chen J, Wei Y, Yang W, Huang Q, Chen Y, Zeng K, et al. IL-6: the link between inflammation, immunity and breast cancer. Front Oncol. 2022;12:903800.
doi: 10.3389/fonc.2022.903800
pubmed: 35924148
pmcid: 9341216
Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, et al. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer. 2003;103:642–6.
doi: 10.1002/ijc.10833
pubmed: 12494472
Zhang GJ, Adachi I. Serum interleukin-6 levels correlate to tumor progression and prognosis in metastatic breast carcinoma. Anticancer Res. 1999;19:1427–32.
pubmed: 10365118
Bachelot T, Ray-Coquard I, Menetrier-Caux C, Rastkha M, Duc A, Blay JY. Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. Br J Cancer. 2003;88:1721–6.
doi: 10.1038/sj.bjc.6600956
pubmed: 12771987
pmcid: 2377148
Ahmad N, Ammar A, Storr SJ, Green AR, Rakha E, Ellis IO, et al. IL-6 and IL-10 are associated with good prognosis in early stage invasive breast cancer patients. Cancer Immunol Immunother. 2018;67:537–49.
doi: 10.1007/s00262-017-2106-8
pubmed: 29256156
Mercogliano MF, Bruni S, Elizalde PV, Schillaci R. Tumor necrosis factor α blockade: an opportunity to tackle breast cancer. Front Oncol. 2020;10:584.
doi: 10.3389/fonc.2020.00584
pubmed: 32391269
pmcid: 7189060
Merendino RA, Arena A, Capozza AB, Chillemi S, Mesiti M. Serum levels of interleukin-10 in patients affected by breast cancer. Immunol Lett. 1996;53:59–60.
doi: 10.1016/0165-2478(96)02598-9
pubmed: 8946219
Hamidullah, Changkija B, Konwar R. Role of interleukin-10 in breast cancer. Breast Cancer Res Treat. 2012;133:11–21.
doi: 10.1007/s10549-011-1855-x
pubmed: 22057973
Baumgarten SC, Frasor J. Minireview: Inflammation: an instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol. 2012;26:360–71.
doi: 10.1210/me.2011-1302
pubmed: 22301780
pmcid: 3286192
Wulaningsih W, Holmberg L, Garmo H, Malmstrom H, Lambe M, Hammar N, et al. Prediagnostic serum inflammatory markers in relation to breast cancer risk, severity at diagnosis and survival in breast cancer patients. Carcinogenesis. 2015;36:1121–8.
doi: 10.1093/carcin/bgv096
pubmed: 26130675
Villaseñor A, Flatt SW, Marinac C, Natarajan L, Pierce JP, Patterson RE. Postdiagnosis C-reactive protein and breast cancer survivorship: findings from the WHEL study. Cancer Epidemiol Biomark Prev. 2014;23:189–99.
doi: 10.1158/1055-9965.EPI-13-0852
Frydenberg H, Thune I, Lofterød T, Mortensen ES, Eggen AE, Risberg T, et al. Pre-diagnostic high-sensitive C-reactive protein and breast cancer risk, recurrence, and survival. Breast Cancer Res Treat. 2016;155:345–54.
doi: 10.1007/s10549-015-3671-1
pubmed: 26740213
Tanaka T, Narazaki M, Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol. 2014;6:a016295.
doi: 10.1101/cshperspect.a016295
pubmed: 25190079
pmcid: 4176007
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.
doi: 10.1038/nature07205
pubmed: 18650914
Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357:539–45.
doi: 10.1016/S0140-6736(00)04046-0
pubmed: 11229684
Harvey AE, Lashinger LM, Hursting SD. The growing challenge of obesity and cancer: an inflammatory issue. Ann N Y Acad Sci. 2011;1229:45–52.
doi: 10.1111/j.1749-6632.2011.06096.x
pubmed: 21793838
Jiralerspong S, Kim ES, Dong W, Feng L, Hortobagyi GN, Giordano SH. Obesity, diabetes, and survival outcomes in a large cohort of early-stage breast cancer patients. Ann Oncol. 2013;24:2506–14.
doi: 10.1093/annonc/mdt224
pubmed: 23793035
pmcid: 3784334
Rao Kondapally Seshasai S, Kaptoge S, Thompson A, Di Angelantonio E, Gao P, Sarwar N, et al. Diabetes mellitus, fasting glucose, and risk of cause-specific death. N Engl J Med. 2011;364:829–41.
doi: 10.1056/NEJMoa1008862
pubmed: 21366474
pmcid: 4109980
Clendenen TV, Arslan AA, Lokshin AE, Idahl A, Hallmans G, Koenig KL, et al. Temporal reliability of cytokines and growth factors in EDTA plasma. BMC Res Notes. 2010;3:302.
doi: 10.1186/1756-0500-3-302
pubmed: 21073739
pmcid: 2997094