Incidence, risk factors and prognostic characteristics of bone metastases and skeletal-related events (SREs) in breast cancer patients: A systematic review of the real world data

Hongwei Zhang, Wei Zhu, Ewelina Biskup, Weige Yang, Ziang Yang, Hong Wang, Xiaochun Qiu, Chengjiao Zhang, Guangxia Hu, Guangfu Hu, Hongwei Zhang, Wei Zhu, Ewelina Biskup, Weige Yang, Ziang Yang, Hong Wang, Xiaochun Qiu, Chengjiao Zhang, Guangxia Hu, Guangfu Hu

Abstract

Purpose: The aim was to systematically extrapolate the occurrence, risk factors, prognostic characteristics, management and outcome of bone metastases (BM) and skeletal related events (SREs) of breast cancer survivors in the real world clinical setting.

Methods: A systematic literature search of PubMed, Web of Science, EMBASE OvidSP and EBSCO Academic Search Complete was conducted. Published prospective and retrospective papers investigating BM and SREs in breast cancer patients in non-trial settings were identified and systematically reviewed.

Results: Twenty-four studies met the inclusion criteria. Incidences of BM based on new diagnosis, length of BM-free interval (BMFI) and number and sites of BM were detected by 17 of 24 studies. Seven studies included in the review were subjected to analyses of risk factors for BM. Developments of SREs regarding the occurrence ratio of total and specific SREs, SERs-free interval (SREFI) and the first-line therapy for SREs were observed in 16 of 24 studies. Out of 5 studies, we extracted uni- and multivariate analysis of risk factor for SREs and out of 16 studies - predictors for survival in breast cancer patients with BM.

Conclusions: BM and SREs are common problems in non-trial breast cancer populations. Patient demographics, clinical stage, tumor pathological type, molecular receptors status are significantly risk factors for incidence of BM, SREs and the survival. The unique characteristics of BM and SREs in breast cancer patients should be taken into account in future randomized controlled trials, as to optimize individual treatment options and assure a maximally long good quality of life.

Keywords: Bone metastases; Breast cancer; Real-world data; Skeletal related events; Systematic review.

Figures

Fig. 1
Fig. 1
PRISMA flow diagram detailing the strategy adopted for the literature search described in this article.

References

    1. Siegel R.L., Miller K.D., Jemal A. Cancer statistics, 2016. CA Cancer J. Clin. 2016;66(1):7–30.
    1. Fan L., Strasser-Weippl K., Li J.J., Louis J. St, Finkelstein D.M., Yu K.D. Breast cancer in China. Lancet Oncol. 2014;15(7):279–289.
    1. Colzani E., Liljegren A., Johansson A.L., Adolfsson J., Hellborg H., Hall P.F. Prognosis of patients with breast cancer: causes of death and effects of time since diagnosis, age, and tumor characteristics. J. Clin. Oncol. 2011;29(30):4014–4021.
    1. McGuire A., Brown J.A., Malone C., McLaughlin R., Kerin M.J. Effects of age on the detection and management of breast cancer. Cancers. 2015;7(2):908–929.
    1. Harris H.R., Bergkvist L., Wolk A. Adherence to the world cancer research fund/american institute for cancer research recommendations and breast cancer risk. Int. J. Cancer. 2016;138(11):2657–2664.
    1. Kellen E., Vansant G., Christiaens M.R., Neven P., Van Limbergen E. Lifestyle changes and breast cancer prognosis: a review. Breast Cancer Res. Treat. 2009;114(1):13–22.
    1. Lim B., Hortobagyi G.N. Current challenges of metastatic breast cancer. Cancer Metastasis Rev. 2016;35(4):495–514.
    1. Senkus E., Łacko A. Over-treatment in metastatic breast cancer. Breast. 2017;31:309–317.
    1. Li S., Peng Y., Weinhandl E.D., Blaes A.H., Cetin K., Chia V.M. Estimated number of prevalent cases of metastatic bone disease in the us adult population. Clin. Epidemiol. 2012;4:87–93.
    1. Mundy G.R. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat. Rev. Cancer. 2002;2(8):584–593.
    1. Manders K., van de Poll-Franse L.V., Creemers G.J., Vreugdenhil G., van der Sangen M.J., Nieuwenhuijzen G.A. Clinical management of women with metastatic breast cancer: a descriptive study according to age group. BMC Cancer. 2006;6:179.
    1. Harries M., Taylor A., Holmberg L., Agbaje O., Garmo H., Kabilan S. Incidence of bone metastases and survival after a diagnosis of bone metastases in breast cancer patients. Cancer Epidemiol. 2014;38(4):427–434.
    1. Svendsen M.L., Gammelager H., Svaerke C., Yong M., Chia V.M., Christiansen C.F. Hospital visits among women with skeletal-related events secondary to breast cancer and bone metastases: a nationwide population-based cohort study in Denmark. Clin. Epidemiol. 2013;5:97–103.
    1. Lipton A., Steger G.G., Figueroa J., Alvarado C., Solal-Celigny P., Body J.J. Randomized active-controlled phase II study of denosumab efficacy and safety in patients with breast cancer-related bone metastases. J. Clin. Oncol. 2007;25(28):4431–4437.
    1. Stopeck A.T., Lipton A., Body J.J., Steger G.G., Tonkin K., de Boer R.H. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study. J. Clin. Oncol. 2010;28(35):5132–5139.
    1. Knobloch K., Yoon U., Vogt P.M. Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias. J. Craniomaxillofac Surg. 2011;39(2):91–92.
    1. Hutton B., Salanti G., Caldwell D.M., Chaimani A., Schmid C.H., Cameron C. The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann. Intern. Med. 2015;162(11):777–784.
    1. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur. J. Epidemiol. 2010;25(9):603–605.
    1. Castillo J.J., Dalia S., Pascual S.K. Association between red blood cell transfusions and development of non-Hodgkin lym- phoma: a meta-analysis of observational studies. Blood. 2010;116:2897–2907.
    1. Liede A., Jerzak K.J., Hernandez R.K., Wade S.W., Sun P., Narod S.A. The incidence of bone metastasis after early-stage breast cancer in Canada. Breast Cancer Res. Treat. 2016;156(3):587–595.
    1. Cetin K., Christiansen C.F., Svaerke C., Jacobsen J.B., Sorensen H.T. Survival in patients with breast cancer with bone metastasis: a Danish population-based cohort study on the prognostic impact of initial stage of disease at breast cancer diagnosis and length of the bone metastasis-free interval. BMJ Open. 2015;5(4):e007702.
    1. Dibekoglu C., Turanli S., Karaman N., Ozcelik K.C., Erdogan O. Bone fracture in breast cancer patients with isolated bone metastasis. Chirugia. 2015;110(1):43–48.
    1. Bollen L., Wibmer C., Wang M., van der Linden Y.M., Leithner A., Bunger C.E. Molecular phenotype is associated with survival in breast cancer patients with spinal bone metastases. Clin. Exp. Metastasis. 2015;32(1):1–5.
    1. Foerster R., Bruckner T., Bostel T., Schlampp I., Debus J., Rief H. Prognostic factors for survival of women with unstable spinal bone metastases from breast cancer. Radiat. Oncol. 2015;10:144.
    1. Harries M., Taylor A., Holmberg L., Agbaje O., Garmo H., Kabilan S. Incidence of bone metastases and survival after a diagnosis of bone metastases in breast cancer patients. Cancer Epidemiol. 2014;38(4):427–434.5.
    1. Steinauer K., Huang D.J., Eppenberger-Castori S., Amann E., Guth U. Bone metastases in breast cancer: frequency, metastatic pattern and non-systemic locoregional therapy. J. Bone Oncol. 2014;3(2):54–60.
    1. Yamashiro H., Takada M., Nakatani E., Imai S., Yamauchi A., Tsuyuki S. Prevalence and risk factors of bone metastasis and skeletal related events in patients with primary breast cancer in Japan. Int J. Clin. Oncol. 2014;19(5):852–862.
    1. Arican A., Bozkurt T., Bozcuk H., Demirkan B., Buyukberber S., Alkis N. A cross-sectional survey of the diagnosis and management of bone metastasis in breast cancer patients in Turkey. Support Care Cancer. 2014;22(10):2629–2634.
    1. Kuchuk I., Hutton B., Moretto P., Ng T., Addison C.L., Clemons M. Incidence, consequences and treatment of bone metastases in breast cancer patients - experience from a single cancer centre. J. Bone Oncol. 2013;2(4):137–144.
    1. Chen J., Zhu S., Xie X.Z., Guo S.F., Tong L.Q., Zhou S. Analysis of clinicopathological factors associated with bone metastasis in breast cancer. J. Huazhong Univ. Sci. Technol. Med. Sci. 2013;33(1):122–125.
    1. Ahn S.G., Lee H.M., Cho S.H., Lee S.A., Hwang S.H., Jeong J. Prognostic factors for patients with bone-only metastasis in breast cancer. Yonsei Med. J. 2013;54(5):1168–1177.
    1. Sathiakumar N., Delzell E., Morrisey M.A., Falkson C., Yong M., Chia V. Mortality following bone metastasis and skeletal-related events among women with breast cancer: a population-based analysis of U.S. Medicare beneficiaries, 1999–2006. Breast Cancer Res. Treat. 2012;131(1):231–238.
    1. Niikura N., Liu J., Hayash N., Palla S.L., Tokuda Y., Hortobagyi G.N. Treatment outcome and prognostic factors for patients with bone-only metastases of breast cancer: a single-institution retrospective analysis. Oncologist. 2011;16(2):155–164.
    1. Lee S.J., Park S., Ahn H.K., Yi J.H., Cho E.Y., Sun J.M. Implications of bone-only metastases in breast cancer: favorable preference with excellent outcomes of hormone receptor positive breast cancer. Cancer Res. Treat. 2011;43(2):89–95.
    1. Koizumi M., Yoshimoto M., Kasumi F., Iwase T. An open cohort study of bone metastasis incidence following surgery in breast cancer patients. BMC Cancer. 2010;10:381.
    1. Trinkaus M., Simmons C., Myers J., Dranatisaris G., Clemons M. Skeletal-related events (SREs) in breast cancer patients with bone metastases treated in the nontrial setting. Support Care Cancer. 2010;18(2):197–203.
    1. Irawan C., Hukom R., Prayogo N. Factors associated with bone metastasis in breast cancer: a preliminary study in an Indonesian population. Acta Med. Indones. 2008;40(4):178–180.
    1. Yavas O., Hayran M., Ozisik Y. Factors affecting survival in breast cancer patients following bone metastasis. Tumori. 2007;93(6):580–586.
    1. Cazzaniga M.E., Dogliotti L., Cascinu S., Barni S., Labianca R., Chiara S. Diagnosis, management and clinical outcome of bone metastases in breast cancer patients: results from a prospective, multicenter study. Oncology. 2006;71(5–6):374–381.
    1. Briasoulis E., Karavasilis V., Kostadima L., Ignatiadis M., Fountzilas G., Pavlidis N. Metastatic breast carcinoma confined to bone: portrait of a clinical entity. Cancer. 2004;101(7):1524–1528.
    1. James J.J., Evans A.J., Pinder S.E., Gutteridge E., Cheung K.L., Chan S. Bone metastases from breast carcinoma: histopathological - radiological correlations and prognostic features. Br. J. Cancer. 2003;89(4):660–665.
    1. Plunkett T.A., Smith P., Rubens R.D. Risk of complications from bone metastases in breast cancer. implications for management. Eur. J. Cancer. 2000;36(4):476–482.
    1. Domchek S.M., Younger J., Finkelstein D.M., Seiden M.V. Predictors of skeletal complications in patients with metastatic breast carcinoma. Cancer. 2000;89(2):363–368.
    1. Baird R.D., Caldas C. Genetic heterogeneity in breast cancer: the road to personalized medicine? BMC Med. 2013;11:151.
    1. Coleman R.E. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin. Cancer Res. 2006;12(20 Pt 2):6243s–6249s.
    1. Coleman R.E., Rubens R.D. The clinical course of bone metastases from breast cancer. Br. J. Cancer. 1987;55(1):61–66.
    1. Group EBCTC, Clarke M., Coates A.S., Darby S.C., Davies C., Gelber R.D. Adjuvant chemotherapy in oestrogen-receptor-poor breast cancer: patient-level meta-analysis of randomised trials. Lancet. 2008;371(9606):29–40.
    1. Houssami N., Costelloe C.M. Imaging bone metastases in breast cancer: evidence on comparative test accuracy. Ann. Oncol. 2012;23(4):834–843.
    1. van der Pol C.B., Schweitzer M.E., Di Primio G., Sampaio M.L., Kielar A., Clemons M. Breast cancer and bone metastases: the association of axial skeleton MRI findings with skeletal-related events and survival. Breast Cancer Res. Treat. 2014;46(3):583–589.
    1. Suva L.J., Griffin R.J., Makhoul I. Mechanisms of bone metastases of breast cancer. Endocr. Relat. Cancer. 2009;16(3):703–713.
    1. Casimiro S., Luis I., Fernandes A., Pires R., Pinto A., Gouveia A.G. Analysis of a bone metastasis gene expression signature in patients with bone metastasis from solid tumors. Clin. Exp. Metastasis. 2012;29(2):155–164.
    1. Lin N.U., Vanderplas A., Hughes M.E., Theriault R.L., Edge S.B., Wong Y.N. Clinicopathologic features, patterns of recurrence, and survival among women with triple-negative breast cancer in the National Comprehensive. Cancer Netw., Cancer. 2012;118(22):5463–5472.
    1. Front D., Schneck S.O., Frankel A., Robinson E. Bone metastases and bone pain in breast cancer. Are they closely associated? JAMA. 1979;242(16):1747–1748.
    1. Sabino M.A., Mantyh P.W. Pathophysiology of bone cancer pain. J. Support Oncol. 2005;3(1):15–24.
    1. Palumbo A., Anderson K. Multiple myeloma. N. Engl. J. Med. 2011;364(11):1046–1060.
    1. Terpos E., Berenson J., Raje N., Roodman G.D. Management of bone disease in multiple myeloma. Expert Rev. Hematol. 2014;7(1):113–125.
    1. Van Poznak C.H., Temin S., Yee G.C., Janjan N.A., Barlow W.E., Biermann J.S. American Society of Clinical O. American Society of Clinical Oncology executive summary of the clinical practice guideline update on the role of bone-modifying agents in metastatic breast cancer. J. Clin. Oncol. 2011;29(9):1221–1227.
    1. Winter M.C., Coleman R.E. Bisphosphonates in the adjuvant treatment of breast cancer. Clin. Oncol. (R. Coll. Radiol.) 2013;25(2):135–145.
    1. Coleman R., de Boer R., Eidtmann H., Llombart A., Davidson N., Neven P. Zoledronic acid (zoledronate) for postmenopausal women with early breast cancer receiving adjuvant letrozole (ZO-FAST study): final 60-month results. Ann. Oncol. 2013;24(2):398–405.
    1. Salmen J., Banys-Paluchowski M., Fehm T. Bone-Targeted Therapy. Geburtshilfe Frauenheilkd. 2015;75(6):584–587.
    1. Delea T.E., Taneja C., Sofrygin O., Kaura S., Gnant M. Cost-effectiveness of zoledronic acid plus endocrine therapy in premenopausal women with hormone-responsive early breast cancer. Clin. Breast Cancer. 2010;10(4):267–274.
    1. Felix J., Andreozzi V., Soares M., Borrego P., Gervasio H., Moreira A. Hospital resource utilization and treatment cost of skeletal-related events in patients with metastatic breast or prostate cancer: estimation for the Portuguese National Health System. Value Health. 2011;14(4):499–505.
    1. Hadji P., Body J.J., Aapro M.S., Brufsky A., Coleman R.E., Guise T. Practical guidance for the management of aromatase inhibitor-associated bone loss. Ann. Oncol. 2008;19(8):1407–1416.
    1. Coleman R.E., Guise T.A., Lipton A., Roodman G.D., Berenson J.R., Body J.J. Advancing treatment for metastatic bone cancer: consensus recommendations from the Second Cambridge Conference. Clin. Cancer Res. 2008;14(20):6387–6395.

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