Skip to main content

Advertisement

SpringerLink
Log in

Myelodysplastic syndrome and acute myeloid leukemia following adjuvant chemotherapy with and without granulocyte colony-stimulating factors for breast cancer

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

Risk of myelodysplastic syndrome (MDS) and acute myeloid leukemia (AML) post-breast cancer treatment with adjuvant chemotherapy and granulocyte colony-stimulating factors (G-CSF) is not fully characterized. Our objective was to estimate MDS/AML risk associated with specific breast cancer treatments. We conducted a retrospective cohort study of women aged ≥66 years with stage I–III breast cancer between 2001 and 2009 using the Surveillance, Epidemiology, and End Results-Medicare database. Women were classified as receiving treatment with radiation, chemotherapy, and/or G-CSF. We used multivariable Cox proportional hazards models to estimate adjusted hazard ratios (HR) and 95 % confidence intervals (CI) for MDS/AML risk. Among 56,251 breast cancer cases, 1.2 % developed MDS/AML during median follow-up of 3.2 years. 47.1 % of women received radiation and 14.3 % received chemotherapy. Compared to breast cancer cases treated with surgery alone, those treated with chemotherapy (HR = 1.38, 95 %-CI 0.98–1.93) and chemotherapy/radiation (HR = 1.77, 95 %-CI 1.25–2.51) had increased risk of MDS/AML, but not radiation alone (HR = 1.08, 95 % CI 0.86–1.36). Among chemotherapy regimens and G-CSF, MDS/AML risk was differentially associated with anthracycline/cyclophosphamide-containing regimens (HR = 1.86, 95 %-CI 1.33–2.61) and filgrastim (HR = 1.47, 95 %-CI 1.05–2.06), but not pegfilgrastim (HR = 1.10, 95 %-CI 0.73–1.66). We observed increased MDS/AML risk among older breast cancer survivors treated with anthracycline/cyclophosphamide chemotherapy that was enhanced by G-CSF. Although small, this risk warrants consideration when determining adjuvant chemotherapy and neutropenia prophylaxis for breast cancer patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Godley LA, Larson RA (2008) Therapy-related myeloid leukemia. Semin Oncol 35(4):418–429. doi:10.1053/j.seminoncol.2008.04.012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Larson RA (2007) Etiology and management of therapy-related myeloid leukemia. Hematol Am Soc Hematol Educ Program. doi:10.1182/asheducation-2007.1.453

    Google Scholar 

  3. Wolff AC, Blackford AL, Visvanathan K, Rugo HS, Moy B, Goldstein LJ, Stockerl-Goldstein K, Neumayer L, Langbaum TS, Theriault RL, Hughes ME, Weeks JC, Karp JE (2015) Risk of marrow neoplasms after adjuvant breast cancer therapy: the national comprehensive cancer network experience. J Clin Oncol 33(4):340–348. doi:10.1200/JCO.2013.54.6119

    Article  PubMed  Google Scholar 

  4. Patt DA, Duan Z, Fang S, Hortobagyi GN, Giordano SH (2007) Acute myeloid leukemia after adjuvant breast cancer therapy in older women: understanding risk. J Clin Oncol 25(25):3871–3876. doi:10.1200/JCO.2007.12.0832

    Article  PubMed  Google Scholar 

  5. Praga C, Bergh J, Bliss J, Bonneterre J, Cesana B, Coombes RC, Fargeot P, Folin A, Fumoleau P, Giuliani R, Kerbrat P, Hery M, Nilsson J, Onida F, Piccart M, Shepherd L, Therasse P, Wils J, Rogers D (2005) Risk of acute myeloid leukemia and myelodysplastic syndrome in trials of adjuvant epirubicin for early breast cancer: correlation with doses of epirubicin and cyclophosphamide. J Clin Oncol 23(18):4179–4191. doi:10.1200/JCO.2005.05.029

    Article  CAS  PubMed  Google Scholar 

  6. Smith RE, Bryant J, DeCillis A, Anderson S (2003) Acute myeloid leukemia and myelodysplastic syndrome after doxorubicin-cyclophosphamide adjuvant therapy for operable breast cancer: the National Surgical Adjuvant Breast and Bowel Project Experience. J Clin Oncol 21(7):1195–1204

    Article  CAS  PubMed  Google Scholar 

  7. Kaplan H, Malmgren J, De Roos AJ (2013) Risk of myelodysplastic syndrome and acute myeloid leukemia post radiation treatment for breast cancer: a population-based study. Breast Cancer Res Treat 137(3):863–867. doi:10.1007/s10549-012-2386-9

    Article  PubMed  Google Scholar 

  8. Kaplan HG, Malmgren JA, Atwood MK (2011) Increased incidence of myelodysplastic syndrome and acute myeloid leukemia following breast cancer treatment with radiation alone or combined with chemotherapy: a registry cohort analysis 1990–2005. BMC Cancer 11:260. doi:10.1186/1471-2407-11-260

    Article  PubMed Central  PubMed  Google Scholar 

  9. Felix CA (1998) Secondary leukemias induced by topoisomerase-targeted drugs. Biochim Biophys Acta 1400(1–3):233–255

    Article  CAS  PubMed  Google Scholar 

  10. Pedersen-Bjergaard J, Pedersen M, Roulston D, Philip P (1995) Different genetic pathways in leukemogenesis for patients presenting with therapy-related myelodysplasia and therapy-related acute myeloid leukemia. Blood 86(9):3542–3552

    CAS  PubMed  Google Scholar 

  11. Du XL, Lairson DR, Begley CE, Fang S (2005) Temporal and geographic variation in the use of hematopoietic growth factors in older women receiving breast cancer chemotherapy: findings from a large population-based cohort. J Clin Oncol 23(34):8620–8628. doi:10.1200/JCO.2005.02.6252

    Article  PubMed Central  PubMed  Google Scholar 

  12. Hershman D, Neugut AI, Jacobson JS, Wang J, Tsai WY, McBride R, Bennett CL, Grann VR (2007) Acute myeloid leukemia or myelodysplastic syndrome following use of granulocyte colony-stimulating factors during breast cancer adjuvant chemotherapy. J Natl Cancer Inst 99(3):196–205. doi:10.1093/jnci/djk028

    Article  CAS  PubMed  Google Scholar 

  13. Lyman GH, Dale DC, Wolff DA, Culakova E, Poniewierski MS, Kuderer NM, Crawford J (2010) Acute myeloid leukemia or myelodysplastic syndrome in randomized controlled clinical trials of cancer chemotherapy with granulocyte colony-stimulating factor: a systematic review. J Clin Oncol 28(17):2914–2924. doi:10.1200/JCO.2009.25.8723

    Article  PubMed  Google Scholar 

  14. Lyman GH (2005) Guidelines of the National Comprehensive Cancer Network on the use of myeloid growth factors with cancer chemotherapy: a review of the evidence. J Natl Compr Cancer Netw 3(4):557–571

    Google Scholar 

  15. Smith TJ, Khatcheressian J, Lyman GH, Ozer H, Armitage JO, Balducci L, Bennett CL, Cantor SB, Crawford J, Cross SJ, Demetri G, Desch CE, Pizzo PA, Schiffer CA, Schwartzberg L, Somerfield MR, Somlo G, Wade JC, Wade JL, Winn RJ, Wozniak AJ, Wolff AC (2006) 2006 update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline. J Clin Oncol 24(19):3187–3205. doi:10.1200/JCO.2006.06.4451

    Article  CAS  PubMed  Google Scholar 

  16. Aapro MS, Bohlius J, Cameron DA, Dal Lago L, Donnelly JP, Kearney N, Lyman GH, Pettengell R, Tjan-Heijnen VC, Walewski J, Weber DC, Zielinski C, European Organisation for R, Treatment of C (2011) 2010 update of EORTC guidelines for the use of granulocyte-colony stimulating factor to reduce the incidence of chemotherapy-induced febrile neutropenia in adult patients with lymphoproliferative disorders and solid tumours. Eur J Cancer 47(1):8–32. doi:10.1016/j.ejca.2010.10.013

    Article  CAS  PubMed  Google Scholar 

  17. Rajan SS, Stearns SC, Lyman GH, Carpenter WR (2011) Effect of primary prophylactic G-CSF use on systemic therapy administration for elderly breast cancer patients. Breast Cancer Res Treat 130(1):255–266. doi:10.1007/s10549-011-1553-8

    Article  CAS  PubMed  Google Scholar 

  18. Kaushansky K (2006) Lineage-specific hematopoietic growth factors. N Engl J Med 354(19):2034–2045. doi:10.1056/NEJMra052706

    Article  CAS  PubMed  Google Scholar 

  19. Citron ML, Berry DA, Cirrincione C, Hudis C, Winer EP, Gradishar WJ, Davidson NE, Martino S, Livingston R, Ingle JN, Perez EA, Carpenter J, Hurd D, Holland JF, Smith BL, Sartor CI, Leung EH, Abrams J, Schilsky RL, Muss HB, Norton L (2003) Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of Intergroup Trial C9741/Cancer and Leukemia Group B Trial 9741. J Clin Oncol 21(8):1431–1439. doi:10.1200/JCO.2003.09.081

    Article  CAS  PubMed  Google Scholar 

  20. Kaplan HG, Malmgren JA, Li CI, Calip GS (2013) Age related risk of myelodysplastic syndrome and acute myeloid leukemia among breast cancer survivors. Breast Cancer Res Treat 142(3):629–636. doi:10.1007/s10549-013-2773-x

    Article  CAS  PubMed  Google Scholar 

  21. Martin MG, Welch JS, Luo J, Ellis MJ, Graubert TA, Walter MJ (2009) Therapy related acute myeloid leukemia in breast cancer survivors, a population-based study. Breast Cancer Res Treat 118(3):593–598. doi:10.1007/s10549-009-0376-3

    Article  PubMed Central  PubMed  Google Scholar 

  22. Schumock GT, Li EC, Suda KJ, Matusiak LM, Hunkler RJ, Vermeulen LC, Hoffman JM (2014) National trends in prescription drug expenditures and projections for 2014. Am J Health-Syst Pharm 71(6):482–499. doi:10.2146/ajhp130767

    Article  PubMed  Google Scholar 

  23. Surveillance Epidemiology and End Results (SEER) Program Overview of the SEER Program http://seer.cancer.gov/about/overview.html

  24. Warren JL, Klabunde CN, Schrag D, Bach PB, Riley GF (2002) Overview of the SEER-Medicare data: content, research applications, and generalizability to the United States elderly population. Med Care 40(8 Suppl):IV-3–IV-18. doi:10.1097/01.MLR.0000020942.47004.03

    Google Scholar 

  25. Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark GM, Edge SB, Hayes DF, Hughes LL, Hutter RV, Morrow M, Page DL, Recht A, Theriault RL, Thor A, Weaver DL, Wieand HS, Greene FL (2003) Staging system for breast cancer: revisions for the 6th edition of the AJCC Cancer Staging Manual. Surg Clin N Am 83(4):803–819. doi:10.1016/S0039-6109(03)00034-3

    Article  PubMed  Google Scholar 

  26. Chubak J, Boudreau DM, Wirtz HS, McKnight B, Weiss NS (2013) Threats to validity of nonrandomized studies of postdiagnosis exposures on cancer recurrence and survival. J Natl Cancer Inst 105(19):1456–1462. doi:10.1093/jnci/djt211

    Article  PubMed Central  PubMed  Google Scholar 

  27. Deyo RA, Cherkin DC, Ciol MA (1992) Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45(6):613–619

    Article  CAS  PubMed  Google Scholar 

  28. Klabunde CN, Potosky AL, Legler JM, Warren JL (2000) Development of a comorbidity index using physician claims data. J Clin Epidemiol 53(12):1258–1267

    Article  CAS  PubMed  Google Scholar 

  29. Bikov KA, Mullins CD, Seal B, Onukwugha E, Hanna N (2013) Algorithm for identifying chemotherapy/biological regimens for metastatic colon cancer in SEER-medicare. Med Care. doi:10.1097/MLR.0b013e31828fad9f

    Google Scholar 

  30. Ma X, Does M, Raza A, Mayne ST (2007) Myelodysplastic syndromes: incidence and survival in the United States. Cancer 109(8):1536–1542. doi:10.1002/cncr.22570

    Article  PubMed  Google Scholar 

  31. Cogle CR, Craig BM, Rollison DE, List AF (2011) Incidence of the myelodysplastic syndromes using a novel claims-based algorithm: high number of uncaptured cases by cancer registries. Blood 117(26):7121–7125. doi:10.1182/blood-2011-02-337964

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Wakeford R (2004) The cancer epidemiology of radiation. Oncogene 23(38):6404–6428. doi:10.1038/sj.onc.1207896

    Article  CAS  PubMed  Google Scholar 

  33. Curtis RE, Boice JD Jr, Stovall M, Bernstein L, Greenberg RS, Flannery JT, Schwartz AG, Weyer P, Moloney WC, Hoover RN (1992) Risk of leukemia after chemotherapy and radiation treatment for breast cancer. N Engl J Med 326(26):1745–1751. doi:10.1056/NEJM199206253262605

    Article  CAS  PubMed  Google Scholar 

  34. Campone M, Roche H, Kerbrat P, Bonneterre J, Romestaing P, Fargeot P, Namer M, Monnier A, Montcuquet P, Goudier MJ, Fumoleau P (2005) Secondary leukemia after epirubicin-based adjuvant chemotherapy in operable breast cancer patients: 16 years experience of the French Adjuvant Study Group. Ann Oncol 16(8):1343–1351. doi:10.1093/annonc/mdi251

    Article  CAS  PubMed  Google Scholar 

  35. Roche H, Fumoleau P, Spielmann M, Canon JL, Delozier T, Serin D, Symann M, Kerbrat P, Soulie P, Eichler F, Viens P, Monnier A, Vindevoghel A, Campone M, Goudier MJ, Bonneterre J, Ferrero JM, Martin AL, Geneve J, Asselain B (2006) Sequential adjuvant epirubicin-based and docetaxel chemotherapy for node-positive breast cancer patients: the FNCLCC PACS 01 Trial. J Clin Oncol 24(36):5664–5671. doi:10.1200/JCO.2006.07.3916

    Article  CAS  PubMed  Google Scholar 

  36. Jones S, Holmes FA, O’Shaughnessy J, Blum JL, Vukelja SJ, McIntyre KJ, Pippen JE, Bordelon JH, Kirby RL, Sandbach J, Hyman WJ, Richards DA, Mennel RG, Boehm KA, Meyer WG, Asmar L, Mackey D, Riedel S, Muss H, Savin MA (2009) Docetaxel with cyclophosphamide is associated with an overall survival benefit compared with doxorubicin and cyclophosphamide: 7-year follow-up of US Oncology Research Trial 9735. J Clin Oncol 27(8):1177–1183. doi:10.1200/JCO.2008.18.4028

    Article  CAS  PubMed  Google Scholar 

  37. Burnell M, Levine MN, Chapman JA, Bramwell V, Gelmon K, Walley B, Vandenberg T, Chalchal H, Albain KS, Perez EA, Rugo H, Pritchard K, O’Brien P, Shepherd LE (2010) Cyclophosphamide, epirubicin, and fluorouracil versus dose-dense epirubicin and cyclophosphamide followed by paclitaxel versus doxorubicin and cyclophosphamide followed by paclitaxel in node-positive or high-risk node-negative breast cancer. J Clin Oncol 28(1):77–82. doi:10.1200/JCO.2009.22.1077

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Tallman MS, Gray R, Bennett JM, Variakojis D, Robert N, Wood WC, Rowe JM, Wiernik PH (1995) Leukemogenic potential of adjuvant chemotherapy for early-stage breast cancer: the Eastern Cooperative Oncology Group experience. J Clin Oncol 13(7):1557–1563

    CAS  PubMed  Google Scholar 

  39. Amgen, Inc. (2013) Neupogen (product monograph). Thousand Oaks: Amgen, Inc

  40. Dong F, Brynes RK, Tidow N, Welte K, Lowenberg B, Touw IP (1995) Mutations in the gene for the granulocyte colony-stimulating-factor receptor in patients with acute myeloid leukemia preceded by severe congenital neutropenia. N Engl J Med 333(8):487–493. doi:10.1056/NEJM199508243330804

    Article  CAS  PubMed  Google Scholar 

  41. Rosenberg PS, Alter BP, Bolyard AA, Bonilla MA, Boxer LA, Cham B, Fier C, Freedman M, Kannourakis G, Kinsey S, Schwinzer B, Zeidler C, Welte K, Dale DC, Severe Chronic Neutropenia International R (2006) The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood 107(12):4628–4635. doi:10.1182/blood-2005-11-4370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Touw IP, Bontenbal M (2007) Granulocyte colony-stimulating factor: key (f)actor or innocent bystander in the development of secondary myeloid malignancy? J Natl Cancer Inst 99(3):183–186. doi:10.1093/jnci/djk057

    Article  CAS  PubMed  Google Scholar 

  43. Naparstek E (1995) Granulocyte colony-stimulating factor, congenital neutropenia, and acute myeloid leukemia. N Engl J Med 333(8):516–518. doi:10.1056/NEJM199508243330811

    Article  CAS  PubMed  Google Scholar 

  44. Shapira MY, Kaspler P, Samuel S, Shoshan S, Or R (2003) Granulocyte colony stimulating factor does not induce long-term DNA instability in healthy peripheral blood stem cell donors. Am J Hematol 73(1):33–36. doi:10.1002/ajh.10324

    Article  CAS  PubMed  Google Scholar 

  45. Confer DL, Miller JP (2007) Long-term safety of filgrastim (rhG-CSF) administration. Br J Haematol 137 (1):77–78; author reply 79–80. doi:10.1111/j.1365-2141.2007.06524.x

  46. Bennett CL, Evens AM, Andritsos LA, Balasubramanian L, Mai M, Fisher MJ, Kuzel TM, Angelotta C, McKoy JM, Vose JM, Bierman PJ, Kuter DJ, Trifilio SM, Devine SM, Tallman MS (2006) Haematological malignancies developing in previously healthy individuals who received haematopoietic growth factors: report from the Research on Adverse Drug Events and Reports (RADAR) project. Br J Haematol 135(5):642–650. doi:10.1111/j.1365-2141.2006.06312.x

    Article  CAS  PubMed  Google Scholar 

  47. Shaw BE, Confer DL, Hwang W, Pulsipher MA (2015) A review of the genetic and long-term effects of G-CSF injections in healthy donors: a reassuring lack of evidence for the development of haematological malignancies. Bone Marrow Transplant 50(3):334–340. doi:10.1038/bmt.2014.278

    Article  CAS  PubMed  Google Scholar 

  48. Slovak ML, Bedell V, Lew D, Albain KS, Ellis GK, Livingston RB, Martino S, Perez EA, Hortobagyi GN, Sher D, Stock W (2010) Screening for clonal hematopoiesis as a predictive marker for development of therapy-related myeloid neoplasia (t-MN) following neoadjuvant therapy for breast cancer: a Southwest Oncology Group study (S0012). Breast Cancer Res Treat 119(2):391–398. doi:10.1007/s10549-009-0597-5

    Article  PubMed Central  PubMed  Google Scholar 

  49. Amgen, Inc. (2013) Neulasta (product monograph). Thousand Oaks: Amgen, Inc

  50. Molineux G, Arvedson T, Foote M (2012) Twenty years of G-CSF: clinical and nonclinical discoveries. Milestones in drug therapy. Springer, Basel

    Book  Google Scholar 

  51. Rizzieri DA, O’Brien JA, Broadwater G, Decastro CM, Dev P, Diehl L, Beaven A, Lagoo A, Gockerman JP, Chao NJ, Moore JO (2009) Outcomes of patients who undergo aggressive induction therapy for secondary acute myeloid leukemia. Cancer 115(13):2922–2929. doi:10.1002/cncr.24379

    Article  PubMed  Google Scholar 

  52. Kroger N, Brand R, van Biezen A, Cahn JY, Slavin S, Blaise D, Sierra J, Zander A, Niederwieser D, de Witte T, Myelodysplastic Syndromes Subcommittee of The Chronic Leukaemia Working Party of the European Group for B, Marrow T (2006) Autologous stem cell transplantation for therapy-related acute myeloid leukemia and myelodysplastic syndrome. Bone Marrow Transplant 37(2):183–189. doi:10.1038/sj.bmt.1705226

    Article  CAS  PubMed  Google Scholar 

  53. Anderson JE, Gooley TA, Schoch G, Anasetti C, Bensinger WI, Clift RA, Hansen JA, Sanders JE, Storb R, Appelbaum FR (1997) Stem cell transplantation for secondary acute myeloid leukemia: evaluation of transplantation as initial therapy or following induction chemotherapy. Blood 89(7):2578–2585

    CAS  PubMed  Google Scholar 

  54. Early Breast Cancer Trialists’ Collaborative G (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365(9472):1687–1717. doi:10.1016/S0140-6736(05)66544-0

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported, in part, by the National Institutes of Health (Contract Number HHSN2612013000121 to the Fred Hutchinson Cancer Research Center) and the Kaplan Cancer Research Fund (J.A.M. and H.G.K.). Author G.S.C. was supported by the National Institutes of Health Cancer Prevention Training Grant in Nutrition, Exercise and Genetics at the University of Washington (R25CA094880).

Author Contributions

G.S.C., J.A.M., S.M.S., and H.G.K. conceived and designed the study; G.S.C., J.A.M., W.J.L., and S.M.S. collected and assembled the data, developed the algorithms, and performed the statistical analyses; all authors interpreted the results and read and commented on the article.

Disclaimers

This study used the linked SEER-Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Program, NCI; the Office of Research, Development and Information, CMS; Information Management Services (IMS), Inc.; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER-Medicare database.

Author information

Authors and Affiliations

  1. Center for Pharmacoepidemiology and Pharmacoeconomic Research, University of Illinois at Chicago, 833 South Wood Street M/C 871, Chicago, IL, 60612-7230, USA

    Gregory S. Calip & Wan-Ju Lee

  2. Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Gregory S. Calip & Stephen M. Schwartz

  3. Department of Epidemiology, University of Washington, Seattle, WA, USA

    Gregory S. Calip, Judith A. Malmgren & Stephen M. Schwartz

  4. HealthStat Consulting, Inc., Seattle, WA, USA

    Judith A. Malmgren

  5. Swedish Cancer Institute, Seattle, WA, USA

    Henry G. Kaplan

Authors
  1. Gregory S. Calip
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Judith A. Malmgren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wan-Ju Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen M. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Henry G. Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory S. Calip.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 47 kb)

Supplementary material 2 (DOCX 48 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Calip, G.S., Malmgren, J.A., Lee, WJ. et al. Myelodysplastic syndrome and acute myeloid leukemia following adjuvant chemotherapy with and without granulocyte colony-stimulating factors for breast cancer. Breast Cancer Res Treat 154, 133–143 (2015). https://doi.org/10.1007/s10549-015-3590-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-015-3590-1

Keywords

Search

Navigation