Abstract
Purpose
Breast cancer is the most common malignancy in women in terms of incidence and mortality. Age is undoubtedly the biggest breast cancer risk factor. In this study we examined clinical, histological, and biological characteristics and mortality of breast cancer in elderly women along with their changes with advancing age.
Methods
We reviewed 63 original articles published between 2006 and 2016 concerning women over 70 years with breast cancer.
Results
Compared to patients 70–79 years, patients aged 80 and over had larger tumor size with fewer T1 (42.9% vs 57.7%, p < 0.01) and more T2 lesions (43.5% vs 33.0%, p < 0.01). Lymph nodes and distant metastases were more frequent, with more N + (49.5% vs 44.0%, p < 0.01) and more M1 (8.0% vs 5.9%, p < 0.01). Infiltrating mucinous carcinomas were more frequent (4.3% vs 3.7%, p < 0.01). Tumors had lower grades, with more grade 1 (23.2% vs 19.8%, p = 0.01) and fewer grade 3 (21.5% vs 25.5%, p < 0.01), and were more hormone-sensitive: PR was more often expressed (72.6% vs 67.3%, p < 0.01). Lympho-vascular invasion was less frequent in the 80 years and over (22.9% vs 29.7%, p = 0.01). Breast cancer-specific mortality was higher both at 5 years (25.8% vs 17.2%, p < 0.01) and 10 years (32.7% vs 26.6%, p < 0.01).
Conclusion
Clinico-pathological characteristics, increased incidence, and mortality associated with aging can be explained on one hand by biological changes of the breast such as increased estrogen sensitivity, epithelial cell alterations, immune senescence, and tumor microenvironment modifications. However, sociologic factors such as increased life expectancy, under-treatment, late diagnosis, and insufficient individual screening, are also involved.
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References
Cancer today IARC (2012) Cancer Fact Sheets: Breast Cancer. World Health Organization. http://gco.iarc.fr/today/fact-sheets-cancers?cancer=15&type=0&sex=2. Accessed October 26, 2016
Protani M, Coory M, Martin JH (2010) Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 123(3):627–635. doi:10.1007/s10549-010-0990-0
Thune I, Brenn T, Lund E, Gaard M (1997) Physical activity and the risk of breast cancer. N Engl J Med 336(18):1269–1275. doi:10.1056/NEJM199705013361801
Beral V, Banks E, Reeves G (2002) Evidence from randomised trials on the long-term effects of hormone replacement therapy. Lancet 360(9337):942–944. doi:10.1016/S0140-6736(02)11032-4
Wacholder S, Hartge P, Prentice R, Garcia-Closas M, Feigelson HS, Diver WR, Thun MJ, Cox DG, Hankinson SE, Kraft P, Rosner B, Berg CD, Brinton LA, Lissowska J, Sherman ME, Chlebowski R, Kooperberg C, Jackson RD, Buckman DW, Hui P, Pfeiffer R, Jacobs KB, Thomas GD, Hoover RN, Gail MH, Chanock SJ, Hunter DJ (2010) Performance of common genetic variants in breast-cancer risk models. N Engl J Med 362(11):986–993. doi:10.1056/NEJMoa0907727
Colonna M, Mitton N, Grosclaude P (2014) Estimation de la prévalence (partielle et totale) du cancer en France métropolitaine chez les 15 ans et plus en 2008 - Étude à partir des registres des cancers du réseau Francim.. Institut de Veille Saniaire. http://www.cancer-environnement.fr/Portals/0/Documents PDF/Estimation-prevalence-cancer-France-metropolitaine-en-2008-2014.pdf. Accessed October 26, 2016
Siegel RL, Miller KD (2016) Jemal A (2016) Cancer statistics. CA Cancer J Clin 66(1):7–30. doi:10.3322/caac.21332
WHO (2016) Definition of an older or elderly person. http://www.who.int/healthinfo/survey/ageingdefnolder/en/. Accessed October 26, 2016
Biganzoli L, Goldhirsch A, Straehle C, Castiglione-Gertsch M, Therasse P, Aapro M, Minisini A, Piccart MJ (2004) Adjuvant chemotherapy in elderly patients with breast cancer: a survey of the Breast International Group (BIG). Ann Oncol 15(2):207–210
Smith BD, Jiang J, McLaughlin SS, Hurria A, Smith GL, Giordano SH, Buchholz TA (2011) Improvement in breast cancer outcomes over time: are older women missing out? J Clin Oncol 29(35):4647–4653. doi:10.1200/JCO.2011.35.8408
Holleczek B, Brenner H (2012) Trends of population-based breast cancer survival in Germany and the US: decreasing discrepancies, but persistent survival gap of elderly patients in Germany. BMC Cancer 12:317. doi:10.1186/1471-2407-12-317
Jensen JD, Cold S, Nielsen MH, Jylling AM, Soe KL, Larsen LB, Ewertz M, Academy of Geriatric Cancer R (2016) Trends in breast cancer in the elderly in Denmark, 1980–2012. Acta Oncol 55(Suppl 1):59–64. doi:10.3109/0284186X.2015.1115118
Molinie F, Vanier A, Woronoff AS, Guizard AV, Delafosse P, Velten M, Daubisse-Marliac L, Arveux P, Tretarre B (2014) Trends in breast cancer incidence and mortality in France 1990–2008. Breast Cancer Res Treat 147(1):167–175. doi:10.1007/s10549-014-3073-9
Cowppli-Bony A, Uhry Z, Remontet L, Guizard A-V, Voirin N, Monnereau A, Bouvier A-M, Colonna M, Bossard N, Woronoff A-S, Grosclaude P (02/2016) Survie des personnes atteintes de cancer en France métropolitaine 1989–2013. Institut de Veille Sanitaire. http://www.e-cancer.fr/content/download/183576/2424633/file/Les_cancers_en_France_en_2016_L_essentiel_des_faits_et_chiffres_mel_20170203.pdf. Accessed August 04, 2017
United Nations Department of Economic and Social Affairs—Population Division (2015) World Population Ageing 2015. United Nations. http://www.un.org/en/development/desa/population/publications/pdf/ageing/WPA2015_Report.pdf. Accessed 26/10/2016
Altobelli E, Rapacchietta L, Angeletti PM, Barbante L, Profeta FV, Fagnano R (2017) Breast cancer screening programmes across the WHO European Region: differences among countries based on national income level. Int J Environ Res Public Health. doi:10.3390/ijerph14040452
Smith RA, Andrews K, Brooks D, DeSantis CE, Fedewa SA, Lortet-Tieulent J, Manassaram-Baptiste D, Brawley OW, Wender RC (2016) Cancer screening in the United States, 2016: a review of current American Cancer Society guidelines and current issues in cancer screening. CA Cancer J Clin 66(2):96–114. doi:10.3322/caac.21336
van de Water W, Markopoulos C, van de Velde CJ, Seynaeve C, Hasenburg A, Rea D, Putter H, Nortier JW, de Craen AJ, Hille ET, Bastiaannet E, Hadji P, Westendorp RG, Liefers GJ, Jones SE (2012) Association between age at diagnosis and disease-specific mortality among postmenopausal women with hormone receptor-positive breast cancer. JAMA 307(6):590–597. doi:10.1001/jama.2012.84
Barthelemy P, Heitz D, Mathelin C, Polesi H, Asmane I, Litique V, Rob L, Bergerat JP, Kurtz JE (2011) Adjuvant chemotherapy in elderly patients with early breast cancer. Impact of age and comprehensive geriatric assessment on tumor board proposals. Crit Rev Oncol Hematol 79(2):196–204. doi:10.1016/j.critrevonc.2010.06.005
Cortadellas T, Cordoba O, Gascon A, Haladjian C, Bernabeu A, Alcalde A, Esgueva A, Rodriguez-Revuelto R, Espinosa-Bravo M, Diaz-Botero S, Xercavins J, Rubio IT, Gil-Moreno A (2015) Surgery improves survival in elderly with breast cancer. A study of 465 patients in a single institution. Eur J Surg Oncol 41(5):635–640. doi:10.1016/j.ejso.2015.01.027
Cyr A, Gillanders WE, Aft RL, Eberlein TJ, Margenthaler JA (2011) Breast cancer in elderly women (≥ 80 years): variation in standard of care? J Surg Oncol 103(3):201–206. doi:10.1002/jso.21799
Dialla PO, Dabakuyo TS, Marilier S, Gentil J, Roignot P, Darut-Jouve A, Poillot ML, Quipourt V, Arveux P (2012) Population-based study of breast cancer in older women: prognostic factors of relative survival and predictors of treatment. BMC Cancer 12:472. doi:10.1186/1471-2407-12-472
Evron E, Goldberg H, Kuzmin A, Gutman R, Rizel S, Sella A, Gutman H (2006) Breast cancer in octogenarians. Cancer 106(8):1664–1668. doi:10.1002/cncr.21788
Eaker S, Dickman PW, Bergkvist L, Holmberg L, Uppsala Orebro Breast, Cancer G (2006) Differences in management of older women influence breast cancer survival: results from a population-based database in Sweden. PLoS Med 3(3):e25. doi:10.1371/journal.pmed.0030025
Li B, Hua B, Lu X, Chen Y, Xiao WZ (2013) Treatment options for elderly breast cancer patients over 70 years old. Zhonghua Yi Xue Za Zhi 93(44):3523–3525
Litvak DA, Arora R (2006) Treatment of elderly breast cancer patients in a community hospital setting. Arch Surg 141 (10):985–990; discussion 990. doi:10.1001/archsurg.141.10.985
Malmgren JA, Parikh J, Atwood MK, Kaplan HG (2014) Improved prognosis of women aged 75 and older with mammography-detected breast cancer. Radiology 273(3):686–694. doi:10.1148/radiol.14140209
Molino A, Giovannini M, Auriemma A, Fiorio E, Mercanti A, Mandara M, Caldara A, Micciolo R, Pavarana M, Cetto GL (2006) Pathological, biological and clinical characteristics, and surgical management, of elderly women with breast cancer. Crit Rev Oncol Hematol 59(3):226–233. doi:10.1016/j.critrevonc.2006.01.007
Niu SH, Jiang YX, Zhu QL, Liu H, Dai Q (2014) Clinical and ultrasonic features of breast cancer in women older than 80 years. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 36(1):57–60. doi:10.3881/j.issn.1000-503X.2014.01.011
Rudra S, Yu DS, Yu ES, Switchenko JM, Mister D, Torres MA (2015) Locoregional and distant recurrence patterns in young versus elderly women treated for breast cancer. Int J Breast Cancer 2015:213123. doi:10.1155/2015/213123
Sanchez RC, Bakal IF, Camus AM, de Besa CP (2013) Characteristics and results of breast cancer in elderly females treated with curative intent. Rev Med Chil 141(12):1534–1540. doi:10.4067/S0034-98872013001200006
Vetter M, Huang DJ, Bosshard G, Guth U (2013) Breast cancer in women 80 years of age and older: a comprehensive analysis of an underreported entity. Acta Oncol 52(1):57–65. doi:10.3109/0284186X.2012.731523
Zhao WH, Xu BH, Li Q, Zhang P, Sun Y (2006) Clinical features and prognosis in breast cancer patients over 70 years of age. Zhonghua Zhong Liu Za Zhi 28(5):385–388
Afsharfard A, Mozaffar M, Orang E, Tahmasbpour E (2013) Trends in epidemiology, clinical and histopathological characteristics of breast cancer in Iran: results of a 17 year study. Asian Pac J Cancer Prev 14(11):6905–6911
Angarita FA, Chesney T, Elser C, Mulligan AM, McCready DR, Escallon J (2015) Treatment patterns of elderly breast cancer patients at two Canadian cancer centres. Eur J Surg Oncol 41(5):625–634. doi:10.1016/j.ejso.2015.01.028
Azim HA Jr, Nguyen B, Brohee S, Zoppoli G, Sotiriou C (2015) Genomic aberrations in young and elderly breast cancer patients. BMC Med 13:266. doi:10.1186/s12916-015-0504-3
Chatzidaki P, Mellos C, Briese V, Mylonas I (2011) Does primary breast cancer in older women (≥ 80 years) have unfavorable histological characteristics? Arch Gynecol Obstet 284(3):705–712. doi:10.1007/s00404-010-1697-5
Cutuli B, Dalenc F, Cottu PH, Gligorov J, Guastalla JP, Petit T, Amrate A (2015) Impact of screening on clinicopathological features and treatment for invasive breast cancer: results of two national surveys. Cancer Radiother 19(5):295–302. doi:10.1016/j.canrad.2015.02.015
Durbecq V, Ameye L, Veys I, Paesmans M, Desmedt C, Sirtaine N, Sotiriou C, Bernard-Marty C, Nogaret JM, Piccart M, Larsimont D (2008) A significant proportion of elderly patients develop hormone-dependant “luminal-B” tumours associated with aggressive characteristics. Crit Rev Oncol Hematol 67(1):80–92. doi:10.1016/j.critrevonc.2007.12.008
Hancke K, Denkinger MD, Konig J, Kurzeder C, Wockel A, Herr D, Blettner M, Kreienberg R (2010) Standard treatment of female patients with breast cancer decreases substantially for women aged 70 years and older: a German clinical cohort study. Ann Oncol 21(4):748–753. doi:10.1093/annonc/mdp364
Kaur P, Santillan AA, McGuire K, Turaga KK, Shamehdi C, Meade T, Ramos D, Mathias M, Parbhoo J, Davis M, Khakpour N, King J, Balducci L, Cox CE (2012) The surgical treatment of breast cancer in the elderly: a single institution comparative review of 5235 patients with 1028 patients ≥ 70 years. Breast J 18(5):428–435. doi:10.1111/j.1524-4741.2012.01272.x
Ma CD, Zhou Q, Nie XQ, Liu GY, Di GH, Wu J, Lu JS, Yang WT, Chen JY, Shao ZM, Shen KW, Shen ZZ (2009) Breast cancer in Chinese elderly women: pathological and clinical characteristics and factors influencing treatment patterns. Crit Rev Oncol Hematol 71(3):258–265. doi:10.1016/j.critrevonc.2008.11.005
Montroni I, Rocchi M, Santini D, Ceccarelli C, Ghignone F, Zattoni D, Nuvola G, Zanotti S, Ugolini G, Taffurelli M (2014) Has breast cancer in the elderly remained the same over recent decades? A comparison of two groups of patients 70 years or older treated for breast cancer twenty years apart. J Geriatr Oncol 5(3):260–265. doi:10.1016/j.jgo.2014.02.006
Pappo I, Karni T, Sandbank J, Dinur I, Sella A, Stahl-Kent V, Wasserman I, Halevy A (2007) Breast cancer in the elderly: histological, hormonal and surgical characteristics. Breast 16(1):60–67. doi:10.1016/j.breast.2006.05.007
Phua CE, Bustam AZ, Yip CH, Taib NA (2010) Prognostic factors for elderly breast cancer patients in University Malaya Medical Centre, Malaysia. Asian Pac J Cancer Prev 11(5):1205–1211
Seah MD, Chan PM (2009) Rethinking undertreatment in elderly breast cancer patients. Asian J Surg 32(2):71–75. doi:10.1016/S1015-9584(09)60013-0
Syed BM, Johnston SJ, Wong DW, Green AR, Winterbottom L, Kennedy H, Simpson N, Morgan DA, Ellis IO, Cheung KL (2012) Long-term (37 years) clinical outcome of older women with early operable primary breast cancer managed in a dedicated clinic. Ann Oncol 23(6):1465–1471. doi:10.1093/annonc/mdr446
Syed BM, Green AR, Paish EC, Soria D, Garibaldi J, Morgan L, Morgan DA, Ellis IO, Cheung KL (2013) Biology of primary breast cancer in older women treated by surgery: with correlation with long-term clinical outcome and comparison with their younger counterparts. Br J Cancer 108(5):1042–1051. doi:10.1038/bjc.2012.601
Tea MK, Tang L, Di GH, Muin D, Steurer S, Delancey JW, Shao ZM, Singer CF (2012) A cross-sectional study of elderly Asian and European women with primary operable breast cancer aged 70 and older. Are there differences? Maturitas 73(3):251–254. doi:10.1016/j.maturitas.2012.08.001
Acevedo F, Camus M, Sanchez C (2015) Breast cancer at extreme ages–a comparative analysis in Chile. Asian Pac J Cancer Prev 16(4):1455–1461
Inal A, Akman T, Yaman S, Ozturk SC, Geredeli C, Bilici M, Inanc M, Harputoglu H, Demirci U, Balakan O, Cinkir HY, Alici S, Colak D, Sonmez OU, Goksel G, Dogu GG, Engin H, Unal OU, Tamozlu T, Buyukberber S, Boruban CM, Isikdogan A (2014) Pathologic and clinical characteristics of elderly patients with breast cancer: a retrospective analysis of a multicenter study (Anatolian Society of Medical Oncology). Int Surg 99(1):2–7. doi:10.9738/INTSURG-D-13-00010
Joerger M, Thurlimann B, Savidan A, Frick H, Rageth C, Lutolf U, Vlastos G, Bouchardy C, Konzelmann I, Bordoni A, Probst-Hensch N, Jundt G, Ess S (2013) Treatment of breast cancer in the elderly: a prospective, population-based Swiss study. J Geriatr Oncol 4(1):39–47. doi:10.1016/j.jgo.2012.08.002
Li JJ, Yu KD, Di GH, Shao ZM (2010) Clinicopathological features and treatment sensitivity of elderly Chinese breast cancer patients. Oncol Lett 1(6):1037–1043. doi:10.3892/ol.2010.179
Tse GM, Tan PH, Lau KM, de Andrade VP, Lui PC, Vong JS, Chaiwun B, Lam CC, Yu AM, Moriya T (2009) Breast cancer in the elderly: a histological assessment. Histopathology 55(4):441–451. doi:10.1111/j.1365-2559.2009.03400.x
Wang J, Kollias J, Boult M, Babidge W, Zorbas HN, Roder D, Maddern G (2010) Patterns of surgical treatment for women with breast cancer in relation to age. Breast J 16(1):60–65. doi:10.1111/j.1524-4741.2009.00828.x
Wildiers H, Van Calster B, van de Poll-Franse LV, Hendrickx W, Roislien J, Smeets A, Paridaens R, Deraedt K, Leunen K, Weltens C, Van Huffel S, Christiaens MR, Neven P (2009) Relationship between age and axillary lymph node involvement in women with breast cancer. J Clin Oncol 27(18):2931–2937. doi:10.1200/JCO.2008.16.7619
Bastiaannet E, Liefers GJ, de Craen AJ, Kuppen PJ, van de Water W, Portielje JE, van der Geest LG, Janssen-Heijnen ML, Dekkers OM, van de Velde CJ, Westendorp RG (2010) Breast cancer in elderly compared to younger patients in the Netherlands: stage at diagnosis, treatment and survival in 127,805 unselected patients. Breast Cancer Res Treat 124(3):801–807. doi:10.1007/s10549-010-0898-8
Hamaker ME, Schreurs WH, Uppelschoten JM, Smorenburg CH (2009) Breast cancer in the elderly: retrospective study on diagnosis and treatment according to national guidelines. Breast J 15(1):26–33. doi:10.1111/j.1524-4741.2008.00667.x
Hartman M, Drotman M, Arleo EK (2015) Annual screening mammography for breast cancer in women 75 years old or older: to screen or not to screen. AJR Am J Roentgenol 204(5):1132–1136. doi:10.2214/AJR.14.13394
Kartal M, Tezcan S, Canda T (2013) Diagnosis, treatment characteristics, and survival of women with breast cancer aged 65 and above: a hospital-based retrospective study. BMC Womens Health 13:34. doi:10.1186/1472-6874-13-34
Orucevic A, Curzon M, Curzon C, Heidel RE, McLoughlin JM, Panella T, Bell J (2015) Breast cancer in elderly caucasian women-an institution-based study of correlation between breast cancer prognostic markers, TNM stage, and overall survival. Cancers (Basel) 7(3):1472–1483. doi:10.3390/cancers7030846
Siegelmann-Danieli N, Khandelwal V, Wood GC, Mainali R, Prichard J, Murphy TJ, Evans JF, Yumen O, Bernath AM (2006) Breast cancer in elderly women: outcome as affected by age, tumor features, comorbidities, and treatment approach. Clin Breast Cancer 7(1):59–66. doi:10.3816/CBC.2006.n.014
Vyas A, Madhavan S, Sambamoorthi U (2014) Association between persistence with mammography screening and stage at diagnosis among elderly women diagnosed with breast cancer. Breast Cancer Res Treat 148(3):645–654. doi:10.1007/s10549-014-3204-3
Albrektsen G, Heuch I, Thoresen SO (2010) Histological type and grade of breast cancer tumors by parity, age at birth, and time since birth: a register-based study in Norway. BMC Cancer 10:226. doi:10.1186/1471-2407-10-226
Anderson WF, Pfeiffer RM, Dores GM, Sherman ME (2006) Comparison of age distribution patterns for different histopathologic types of breast carcinoma. Cancer Epidemiol Biomark Prev 15(10):1899–1905. doi:10.1158/1055-9965.EPI-06-0191
Cheung KL, Wong AW, Parker H, Li VW, Winterbottom L, Morgan DA, Ellis IO (2008) Pathological features of primary breast cancer in the elderly based on needle core biopsies–a large series from a single centre. Crit Rev Oncol Hematol 67(3):263–267. doi:10.1016/j.critrevonc.2008.04.002
Mathew J, Lee S, Syed BM, Morgan DA, Ellis IO, Cheung KL (2014) A study of ductal versus non-ductal invasive breast carcinomas in older women: long-term clinical outcome and comparison with their younger counterparts. Breast Cancer Res Treat 147(3):671–674. doi:10.1007/s10549-014-3094-4
Roder D, Wang JX, Zorbas H, Kollias J, Maddern G (2010) Survival from breast cancers managed by surgeons participating in the National Breast Cancer Audit of the Royal Australasian College of Surgeons. ANZ J Surg 80(11):776–780. doi:10.1111/j.1445-2197.2010.05341.x
Clough-Gorr KM, Thwin SS, Stuck AE, Silliman RA (2012) Examining five- and ten-year survival in older women with breast cancer using cancer-specific geriatric assessment. Eur J Cancer 48(6):805–812. doi:10.1016/j.ejca.2011.06.016
Patnaik JL, Byers T, Diguiseppi C, Denberg TD, Dabelea D (2011) The influence of comorbidities on overall survival among older women diagnosed with breast cancer. J Natl Cancer Inst 103(14):1101–1111. doi:10.1093/jnci/djr188
Haque R, Ahmed SA, Inzhakova G, Shi J, Avila C, Polikoff J, Bernstein L, Enger SM, Press MF (2012) Impact of breast cancer subtypes and treatment on survival: an analysis spanning two decades. Cancer Epidemiol Biomark Prev 21(10):1848–1855. doi:10.1158/1055-9965.EPI-12-0474
Diab SG, Elledge RM, Clark GM (2000) Tumor characteristics and clinical outcome of elderly women with breast cancer. J Natl Cancer Inst 92(7):550–556
Goss PE, Ingle JN, Pritchard KI, Robert NJ, Muss H, Gralow J, Gelmon K, Whelan T, Strasser-Weippl K, Rubin S, Sturtz K, Wolff AC, Winer E, Hudis C, Stopeck A, Beck JT, Kaur JS, Whelan K, Tu D, Parulekar WR (2016) Extending aromatase-inhibitor adjuvant therapy to 10 years. N Engl J Med 375(3):209–219. doi:10.1056/NEJMoa1604700
Collaborative Group on Hormonal Factors in Breast C (2012) Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol 13(11):1141–1151. doi:10.1016/S1470-2045(12)70425-4
Savolainen-Peltonen H, Vihma V, Leidenius M, Wang F, Turpeinen U, Hamalainen E, Tikkanen MJ, Mikkola TS (2014) Breast adipose tissue estrogen metabolism in postmenopausal women with or without breast cancer. J Clin Endocrinol Metab 99(12):E2661–E2667. doi:10.1210/jc.2014-2550
Darbre PD (2014) Hypersensitivity and growth adaptation of oestrogen-deprived MCF-7 human breast cancer cells. Anticancer Res 34(1):99–105
Sogaard M, Farkas DK, Ehrenstein V, Jorgensen JO, Dekkers OM, Sorensen HT (2016) Hypothyroidism and hyperthyroidism and breast cancer risk: a nationwide cohort study. Eur J Endocrinol 174(4):409–414. doi:10.1530/EJE-15-0989
Russo J, Russo IH (2004) Development of the human breast. Maturitas 49(1):2–15. doi:10.1016/j.maturitas.2004.04.011
Balducci L (2000) Geriatric oncology: challenges for the new century. Eur J Cancer 36(14):1741–1754
Raynaud CM, Hernandez J, Llorca FP, Nuciforo P, Mathieu MC, Commo F, Delaloge S, Sabatier L, Andre F, Soria JC (2010) DNA damage repair and telomere length in normal breast, preneoplastic lesions, and invasive cancer. Am J Clin Oncol 33(4):341–345. doi:10.1097/COC.0b013e3181b0c4c2
Radisky DC, Visscher DW, Frank RD, Vierkant RA, Winham S, Stallings-Mann M, Hoskin TL, Nassar A, Vachon CM, Denison LA, Hartmann LC, Frost MH, Degnim AC (2016) Natural history of age-related lobular involution and impact on breast cancer risk. Breast Cancer Res Treat 155(3):423–430. doi:10.1007/s10549-016-3691-5
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. doi:10.1016/j.cell.2011.02.013
Spaeth EL, Labaff AM, Toole BP, Klopp A, Andreeff M, Marini FC (2013) Mesenchymal CD44 expression contributes to the acquisition of an activated fibroblast phenotype via TWIST activation in the tumor microenvironment. Cancer Res 73(17):5347–5359. doi:10.1158/0008-5472.CAN-13-0087
Collado M, Blasco MA, Serrano M (2007) Cellular senescence in cancer and aging. Cell 130(2):223–233. doi:10.1016/j.cell.2007.07.003
Aifuwa I, Giri A, Longe N, Lee SH, An SS, Wirtz D (2015) Senescent stromal cells induce cancer cell migration via inhibition of RhoA/ROCK/myosin-based cell contractility. Oncotarget 6(31):30516–30531. doi:10.18632/oncotarget.5854
Pazolli E, Luo X, Brehm S, Carbery K, Chung JJ, Prior JL, Doherty J, Demehri S, Salavaggione L, Piwnica-Worms D, Stewart SA (2009) Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Res 69(3):1230–1239. doi:10.1158/0008-5472.CAN-08-2970
Erez N, Truitt M, Olson P, Arron ST, Hanahan D (2010) Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 17(2):135–147. doi:10.1016/j.ccr.2009.12.041
Bussard KM, Mutkus L, Stumpf K, Gomez-Manzano C, Marini FC (2016) Tumor-associated stromal cells as key contributors to the tumor microenvironment. Breast Cancer Res 18(1):84. doi:10.1186/s13058-016-0740-2
Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21(3):309–322. doi:10.1016/j.ccr.2012.02.022
Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt MR, Romero IL, Carey MS, Mills GB, Hotamisligil GS, Yamada SD, Peter ME, Gwin K, Lengyel E (2011) Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 17(11):1498–1503. doi:10.1038/nm.2492
Motrescu ER, Rio MC (2008) Cancer cells, adipocytes and matrix metalloproteinase 11: a vicious tumor progression cycle. Biol Chem 389(8):1037–1041. doi:10.1515/BC.2008.110
Hefetz-Sela S, Scherer PE (2013) Adipocytes: impact on tumor growth and potential sites for therapeutic intervention. Pharmacol Ther 138(2):197–210. doi:10.1016/j.pharmthera.2013.01.008
Tan J, Buache E, Chenard MP, Dali-Youcef N, Rio MC (2011) Adipocyte is a non-trivial, dynamic partner of breast cancer cells. Int J Dev Biol 55(7–9):851–859. doi:10.1387/ijdb.113365jt
Andarawewa KL, Motrescu ER, Chenard MP, Gansmuller A, Stoll I, Tomasetto C, Rio MC (2005) Stromelysin-3 is a potent negative regulator of adipogenesis participating to cancer cell-adipocyte interaction/crosstalk at the tumor invasive front. Cancer Res 65(23):10862–10871. doi:10.1158/0008-5472.CAN-05-1231
Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, Wang YY, Meulle A, Salles B, Le Gonidec S, Garrido I, Escourrou G, Valet P, Muller C (2011) Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res 71(7):2455–2465. doi:10.1158/0008-5472.CAN-10-3323
Rio MC, Dali-Youcef N, Tomasetto C (2015) Local adipocyte cancer cell paracrine loop: can “sick fat” be more detrimental? Horm Mol Biol Clin Investig 21(1):43–56. doi:10.1515/hmbci-2014-0044
Kimijima I, Ohtake T, Sagara H, Watanabe T, Takenoshita S (2000) Scattered fat invasion: an indicator for poor prognosis in premenopausal, and for positive estrogen receptor in postmenopausal breast cancer patients. Oncology 59(Suppl 1):25–30.
Yamaguchi J, Ohtani H, Nakamura K, Shimokawa I, Kanematsu T (2008) Prognostic impact of marginal adipose tissue invasion in ductal carcinoma of the breast. Am J Clin Pathol 130(3):382–388. doi:10.1309/MX6KKA1UNJ1YG8VN
Wang YY, Lehuede C, Laurent V, Dirat B, Dauvillier S, Bochet L, Le Gonidec S, Escourrou G, Valet P, Muller C (2012) Adipose tissue and breast epithelial cells: a dangerous dynamic duo in breast cancer. Cancer Lett 324(2):142–151. doi:10.1016/j.canlet.2012.05.019
Gruver A, Hudson L, Sempowski G (2007) Immunosenescence of ageing. J Pathol 211(2):144–156
Falci C, Gianesin K, Sergi G, Giunco S, De Ronch I, Valpione S, Solda C, Fiduccia P, Lonardi S, Zanchetta M, Keppel S, Brunello A, Zafferri V, Manzato E, De Rossi A, Zagonel V (2013) Immune senescence and cancer in elderly patients: results from an exploratory study. Exp Gerontol 48(12):1436–1442. doi:10.1016/j.exger.2013.09.011
Petkov VI, Miller DP, Howlader N, Gliner N, Howe W, Schussler N, Cronin K, Baehner FL, Cress R, Deapen D, Glaser SL, Hernandez BY, Lynch CF, Mueller L, Schwartz AG, Schwartz SM, Stroup A, Sweeney C, Tucker TC, Ward KC, Wiggins C, Wu XC, Penberthy L, Shak S (2016) Breast-cancer-specific mortality in patients treated based on the 21-gene assay: a SEER population-based study. NPJ Breast Cancer 2:16017. doi:10.1038/npjbcancer.2016.17
Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: the challenges ahead. Lancet 374(9696):1196–1208. doi:10.1016/S0140-6736(09)61460-4
Rogel A, Hamers F, Quintin C, de Maria F, Bonaldi C, Beltzer N (2016) Breast cancer in France: incidence and screening. Santé Publique France. http://invs.santepubliquefrance.fr/Publications-et-outils/Rapports-et-syntheses/Maladies-chroniques-et-traumatismes/2016/Incidence-et-depistage-du-cancer-du-sein-en-France
Larson KE, Cowher MS, O’Rourke C, Patel M, Pratt D (2016) Do primary care physician perform clinical breast exams prior to ordering a mammogram? Breast J 22(2):189–193. doi:10.1111/tbj.12546
Steptoe A, Shankar A, Demakakos P, Wardle J (2013) Social isolation, loneliness, and all-cause mortality in older men and women. Proc Natl Acad Sci U S A 110(15):5797–5801. doi:10.1073/pnas.1219686110
Giordano SH, Hortobagyi GN, Kau SW, Theriault RL, Bondy ML (2005) Breast cancer treatment guidelines in older women. J Clin Oncol 23(4):783–791. doi:10.1200/JCO.2005.04.175
Bouchardy C, Rapiti E, Fioretta G, Laissue P, Neyroud-Caspar I, Schafer P, Kurtz J, Sappino AP, Vlastos G (2003) Undertreatment strongly decreases prognosis of breast cancer in elderly women. J Clin Oncol 21(19):3580–3587. doi:10.1200/JCO.2003.02.046
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We thank Dr. Andrea Lodi Ph.D., for the help with the English translation and Dr. Shanti Amé M.D., for the careful corrections of the manuscript.
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Lodi, M., Scheer, L., Reix, N. et al. Breast cancer in elderly women and altered clinico-pathological characteristics: a systematic review. Breast Cancer Res Treat 166, 657–668 (2017). https://doi.org/10.1007/s10549-017-4448-5
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DOI: https://doi.org/10.1007/s10549-017-4448-5