Optimal use of granulocyte colony-stimulating factor prophylaxis to improve survival in cancer patients receiving treatment : An expert view.
Cancer supportive care
Chemotherapy dose intensity
Febrile neutropenia
G-CSF prophylaxis
Journal
Wiener klinische Wochenschrift
ISSN: 1613-7671
Titre abrégé: Wien Klin Wochenschr
Pays: Austria
ID NLM: 21620870R
Informations de publication
Date de publication:
27 Nov 2023
27 Nov 2023
Historique:
received:
15
09
2023
accepted:
09
10
2023
medline:
27
11
2023
pubmed:
27
11
2023
entrez:
27
11
2023
Statut:
aheadofprint
Résumé
Febrile neutropenia (FN) is a relatively common complication of cytotoxic chemotherapy. Prophylaxis with granulocyte colony-stimulating factor (G-CSF) can prevent FN and chemotherapy dose delays and enable the use of the higher dose intensities associated with a survival benefit; however, G‑CSF is not always used optimally. Five medical oncologists with a special interest in supportive care met to discuss the evidence for prophylaxis with G‑CSF to improve survival in cancer patients, identify reasons why this is not always done, and suggest potential solutions. The dose intensity of chemotherapy is critical for maximizing survival in cancer patients but may be reduced as a result of hematological toxicity, such as FN. Use of G‑CSF has been shown to increase the chances of achieving the planned dose intensity in various cancers, including early-stage breast cancer and non-Hodgkin lymphoma. All physicians treating cancer patients should consider the use of G‑CSF prophylaxis in patients receiving chemotherapy, paying particular attention to patient-related risk factors. Strategies to optimize G‑CSF use include educating medical oncologists and pharmacists on the appropriate use of G‑CSF and informing patients about the efficacy of G‑CSF and its potential adverse effects. It is hoped that the evidence and opinions presented will help to encourage appropriate use of G‑CSF to support cancer patients at risk of FN in achieving the best possible outcomes from chemotherapy.
Sections du résumé
BACKGROUND
BACKGROUND
Febrile neutropenia (FN) is a relatively common complication of cytotoxic chemotherapy. Prophylaxis with granulocyte colony-stimulating factor (G-CSF) can prevent FN and chemotherapy dose delays and enable the use of the higher dose intensities associated with a survival benefit; however, G‑CSF is not always used optimally. Five medical oncologists with a special interest in supportive care met to discuss the evidence for prophylaxis with G‑CSF to improve survival in cancer patients, identify reasons why this is not always done, and suggest potential solutions. The dose intensity of chemotherapy is critical for maximizing survival in cancer patients but may be reduced as a result of hematological toxicity, such as FN. Use of G‑CSF has been shown to increase the chances of achieving the planned dose intensity in various cancers, including early-stage breast cancer and non-Hodgkin lymphoma. All physicians treating cancer patients should consider the use of G‑CSF prophylaxis in patients receiving chemotherapy, paying particular attention to patient-related risk factors.
KEY MESSAGES
CONCLUSIONS
Strategies to optimize G‑CSF use include educating medical oncologists and pharmacists on the appropriate use of G‑CSF and informing patients about the efficacy of G‑CSF and its potential adverse effects. It is hoped that the evidence and opinions presented will help to encourage appropriate use of G‑CSF to support cancer patients at risk of FN in achieving the best possible outcomes from chemotherapy.
Identifiants
pubmed: 38010512
doi: 10.1007/s00508-023-02300-6
pii: 10.1007/s00508-023-02300-6
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Klastersky J, de Naurois J, Rolston K, Rapoport B, Maschmeyer G, Aapro M, Herrstedt J; the ESMO Guidelines Committee. Management of febrile neutropaenia: ESMO Clinical Practice Guidelines. Ann Oncol. 2016;27:v111–8.
doi: 10.1093/annonc/mdw325
Aagaard T, Reekie J, Jorgensen M, Roen A, Daugaard G, Specht L, et al. Mortality and admission to intensive care units after febrile neutropenia in patients with cancer. Cancer Med. 2020;9(9):3033–42.
doi: 10.1002/cam4.2955
pubmed: 32144897
pmcid: 7196064
U.S. Department of Health and Human Resources. Common Terminology Criteria for Adverse Events (CTCAE). Version 5.0. 2017. Available from: https://ctep.cancer.gov/protocoldevelopment/electronic_applications/docs/ctcae_v5_quick_reference_5x7.pdf
Kuderer NM, Dale DC, Crawford J, Cosler LE, Lyman GH. Mortality, morbidity, and cost associated with febrile neutropenia in adult cancer patients. Cancer. 2006;106(10):2258–66.
doi: 10.1002/cncr.21847
pubmed: 16575919
Li Y, Klippel Z, Shih X, Reiner M, Wang H, Page JH. Relationship between severity and duration of chemotherapy-induced neutropenia and risk of infection among patients with nonmyeloid malignancies. Support Care Cancer. 2016;24:4377–83.
doi: 10.1007/s00520-016-3277-0
pubmed: 27278272
Tai E, Guy GP, Dunbar A, Richardson LC. Cost of cancer-related neutropenia or fever hospitalizations, United States, 2012. J Oncol Pract. 2017;13(6):e552–e61.
doi: 10.1200/JOP.2016.019588
pubmed: 28437150
pmcid: 5470648
Averin A, Silvia A, Lamerato L, Richert-Boe K, Kaur M, Sundaresan D, et al. Risk of chemotherapy-induced febrile neutropenia in patients with metastatic cancer not receiving granulocyte colony-stimulating factor prophylaxis in US clinical practice. Support Care Cancer. 2021;29(4):2179–86.
doi: 10.1007/s00520-020-05715-3
pubmed: 32880732
Crawford J, Ozer H, Stoller R, Johnson D, Lyman G, Tabbara I, et al. Reduction by granulocyte colony-stimulating factor of fever and neutropenia induced by chemotherapy in patients with small-cell lung cancer. N Engl J Med. 1991;325(3):164–70.
doi: 10.1056/NEJM199107183250305
pubmed: 1711156
American Society of Clinical Oncology. Recommendations for the use of hematopoietic colony-stimulating factors: evidence-based, clinical practice guidelines. J Clin Oncol. 1994;12(11):2471–508.
doi: 10.1200/JCO.1994.12.11.2471
Ozer H, Armitage JO, Bennett CL, Crawford J, Demetri GD, Pizzo PA, et al. 2000 update of recommendations for the use of hematopoietic colony-stimulating factors: evidence-based, clinical practice guidelines. American Society of Clinical Oncology Growth Factors Expert Panel. J Clin Oncol. 2000;18(20):3558–85.
doi: 10.1200/JCO.2000.18.20.3558
pubmed: 11032599
Vogel CL, Wojtukiewicz MZ, Carroll RR, Tjulandin SA, Barajas-Figueroa LJ, Wiens BL, et al. First and subsequent cycle use of pegfilgrastim prevents febrile neutropenia in patients with breast cancer: a multicenter, double-blind, placebo-controlled phase III study. J Clin Oncol. 2005;23(6):1178–84.
doi: 10.1200/JCO.2005.09.102
pubmed: 15718314
National Comprehensive Cancer Network. NCCN Guidelines for Hematopoietic Growth Factors. Version 2. 2023. Available from: www.nccn.org/guidelines/guidelines-detail?category=3&id=1493
Aapro MS, Bohlius J, Cameron DA, Dal Lago L, Donnelly JP, Kearney N, et al. 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. 2011;47(1):8–32.
doi: 10.1016/j.ejca.2010.10.013
pubmed: 21095116
Smith TJ, Bohlke K, Lyman GH, Carson KR, Crawford J, Cross SJ, et al. Recommendations for the use of WBC growth factors: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2015;33(28):3199–212.
doi: 10.1200/JCO.2015.62.3488
pubmed: 26169616
European Society for Medical Oncology. Supportive care strategies during the COVID-19 pandemic. Available from: www.esmo.org/guidelines/cancer-patient-management-during-the-covid-19-pandemic/supportive-care-in-the-covid-19-era
Prabhakar M, Ershler WB, Longo DL. Bone marrow, thymus and blood: changes across the lifespan. Aging Health. 2009;5:385–93.
doi: 10.2217/ahe.09.31
Link H, Kerkmann M, Holtmann L, Ortner P. G‑CSF guideline adherence in Germany, an update with a retrospective and representative sample survey. Support Care Cancer. 2019;27(4):1459–69.
doi: 10.1007/s00520-018-4481-x
pubmed: 30374765
Bonadonna G, Valagussa P, Moliterni A, Zambetti M, Brambilla C. Adjuvant cyclophosphamide, methotrexate, and fluorouracil in node-positive breast cancer: the results of 20 years of follow-up. N Engl J Med. 1995;332(14):901–6.
doi: 10.1056/NEJM199504063321401
pubmed: 7877646
Chirivella I, Bermejo B, Insa A, Perez-Fidalgo A, Magro A, Rosello S, et al. Optimal delivery of anthracycline-based chemotherapy in the adjuvant setting improves outcome of breast cancer patients. Breast Cancer Res Treat. 2009;114(3):479–84.
doi: 10.1007/s10549-008-0018-1
pubmed: 18463977
Leonard RC, Mansi JL, Keerie C, Yellowlees A, Crawford S, Benstead K, et al. A randomised trial of secondary prophylaxis using granulocyte colony-stimulating factor (’SPROG’ trial) for maintaining dose intensity of standard adjuvant chemotherapy for breast cancer by the Anglo-Celtic Cooperative Group and NCRN. Ann Oncol. 2015;26(12):2437–41.
doi: 10.1093/annonc/mdv389
pubmed: 26416895
Del Mastro L, Poggio F, Blondeaux E, De Placido S, Giuliano M, Forestieri V, et al. Fluorouracil and dose-dense adjuvant chemotherapy in patients with early-stage breast cancer (GIM2): end-of-study results from a randomised, phase 3 trial. Lancet Oncol. 2022;23(12):1571–82.
doi: 10.1016/S1470-2045(22)00632-5
pubmed: 36370716
Bosly A, Bron D, Van Hoof A, De Bock R, Berneman Z, Ferrant A, et al. Achievement of optimal average relative dose intensity and correlation with survival in diffuse large B‑cell lymphoma patients treated with CHOP. Ann Hematol. 2008;87(4):277–83.
doi: 10.1007/s00277-007-0399-y
pubmed: 17952688
Pettengell R, Schwenkglenks M, Bosly A. Association of reduced relative dose intensity and survival in lymphoma patients receiving CHOP-21 chemotherapy. Ann Hematol. 2008;87(5):429–30.
doi: 10.1007/s00277-008-0447-2
pubmed: 18299833
pmcid: 2275304
Pfreundschuh M, Trumper L, Kloess M, Schmits R, Feller AC, Rube C, et al. Two-weekly or 3‑weekly CHOP chemotherapy with or without etoposide for the treatment of elderly patients with aggressive lymphomas: results of the NHL-B2 trial of the DSHNHL. Blood. 2004;104(3):634–41.
doi: 10.1182/blood-2003-06-2095
pubmed: 15016643
Pfreundschuh M, Trumper L, Kloess M, Schmits R, Feller AC, Rudolph C, et al. Two-weekly or 3‑weekly CHOP chemotherapy with or without etoposide for the treatment of young patients with good-prognosis (normal LDH) aggressive lymphomas: results of the NHL-B1 trial of the DSHNHL. Blood. 2004;104(3):626–33.
doi: 10.1182/blood-2003-06-2094
pubmed: 14982884
Brusamolino E, Rusconi C, Montalbetti L, Gargantini L, Uziel L, Pinotti G, et al. Dose-dense R‑CHOP-14 supported by pegfilgrastim in patients with diffuse large B‑cell lymphoma: a phase II study of feasibility and toxicity. Haematologica. 2006;91(4):496–502.
pubmed: 16537117
Moore DC. Drug-induced neutropenia: a focus on rituximab-induced late-onset neutropenia. P T. 2016;41(12:765–8.
Al-Batran SE, Homann N, Pauligk C, Goetze TO, Meiler J, Kasper S, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet. 2019;393(10184):1948–57.
doi: 10.1016/S0140-6736(18)32557-1
pubmed: 30982686
ClinicalTrials.gov. Phase II study of atezolizumab + FLOT vs. FLOT alone in patients with gastric cancer and GEJ (DANTE). Available from: https://clinicaltrials.gov/ct2/show/NCT03421288
Al-Batran SE, Lorenzen S, Thuss-Patience PC, Homann N, Schenk M, Lindig U, et al. Surgical and pathological outcome, and pathological regression, in patients receiving perioperative atezolizumab in combination with FLOT chemotherapy versus FLOT alone for resectable esophagogastric adenocarcinoma: Interim results from DANTE, a randomized, multicenter, phase IIb trial of the FLOT-AIO German Gastric Cancer Group and Swiss SAKK. J Clin Oncol. 2022;40:4003.
doi: 10.1200/JCO.2022.40.16_suppl.4003
Canton C, Boussari O, Boulin M, Le Malicot K, Taieb J, Dahan L, et al. Impact of G‑CSF prophylaxis on chemotherapy dose-intensity, link between dose-intensity and survival in patients with metastatic pancreatic adenocarcinoma. Oncologist. 2022;27(7):e571–e9.
doi: 10.1093/oncolo/oyac055
pubmed: 35289915
pmcid: 9255980
Lyman GH, Yau L, Nakov R, Krendyukov A. Overall survival and risk of second malignancies with cancer chemotherapy and G‑CSF support. Ann Oncol. 2018;29(9):1903–10.
doi: 10.1093/annonc/mdy311
pubmed: 30099478
Truong J, Lee EK, Trudeau ME, Chan KK. Interpreting febrile neutropenia rates from randomized, controlled trials for consideration of primary prophylaxis in the real world: a systematic review and meta-analysis. Ann Oncol. 2016;27(4):608–18.
doi: 10.1093/annonc/mdv619
pubmed: 26712901
Hawkins A, Murphy A, McNamara M, Gawade PL, Belani R, Kelsh MA. A survey of oncologists’ perceptions and opinions regarding the use of granulocyte colony-stimulating factors. J Cancer Educ. 2020;35(1):178–86.
doi: 10.1007/s13187-019-01638-8
pubmed: 31656028
Zullo AR, Lou U, Cabral SE, Huynh J, Berard-Collins CM. Overuse and underuse of pegfilgrastim for primary prophylaxis of febrile neutropenia. J Oncol Pharm Pract. 2019;25(6):1357–65.
doi: 10.1177/1078155218792698
pubmed: 30124123
Dittrich CK, Kosty M, Jezdic S, Pyle D, Berardi R, Bergh J, et al. ESMO / ASCO recommendations for a global curriculum in medical oncology edition. Esmo Open. 2016;2016(1):e97.
Bernens JN, Hartman K, Curley B, Wen S, Rogers J, Abraham J, et al. Assessing the impact of a targeted electronic medical record intervention on the use of growth factor in cancer patients. J Community Support Oncol. 2015;13(3):113–6.
doi: 10.12788/jcso.0117
pubmed: 26287033
pmcid: 4792513
European Medicines Agency. Ziextenzo. Summary of Product Characteristics. Published 2019. Available From: wwwe.ema.europa.eu/en/documents/product-information/ziextenzo-epar-product-information_en.pdf.
European Medicines Agency. Zarzio. Summary of Product Characteristics. Updated 2022. Available from: https://www.ema.europa.eu/en/documents/product-information/zarzio-epar-product-information_en.pdf
McCullough J, Clay M, Herr G, Smith J, Stroncek D. Effects of granulocyte-colony-stimulating factor on potential normal granulocyte donors. Transfusion. 1999;39(10):1136–40.
doi: 10.1046/j.1537-2995.1999.39101136.x
pubmed: 10532609
Lyman GH, Dale DC, Wolff DA, Culakova E, Poniewierski MS, Kuderer NM, et al. 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. 2010;28(17):2914–24.
doi: 10.1200/JCO.2009.25.8723
pubmed: 20385991
Cornes P, Gascon P, Vulto AG, Aapro M. Biosimilar pegfilgrastim: improving access and optimising practice to supportive care that enables cure. BioDrugs. 2020;34(3):255–63.
doi: 10.1007/s40259-020-00411-4
pubmed: 32232676
pmcid: 7211191
Li E, Mezzio DJ, Campbell D, Campbell K, Lyman GH. Primary prophylaxis with biosimilar filgrastim for patients at intermediate risk for febrile neutropenia: a cost-effectiveness analysis. Jco Oncol Pract. 2021;17(8):e1235–e45.
doi: 10.1200/OP.20.01047
pubmed: 33793342
pmcid: 8360497
Roche H, Eymard JC, Radji A, Prevost A, Diab R, Lamuraglia M, et al. Biosimilar filgrastim treatment patterns and prevention of febrile neutropenia: a prospective multicentre study in France in patients with solid tumours (the ZOHe study). BMC. Cancer. 2018;18(1):1127.
pubmed: 30445935
pmcid: 6240200