Systematic Review
. 2008 Oct; (4):CD003189.
doi: 10.1002/14651858.CD003189.pub4.

Granulopoiesis-stimulating factors to prevent adverse effects in the treatment of malignant lymphoma

Julia Bohlius 1 Christine Herbst  Marcel Reiser  Guido Schwarzer  Andreas Engert  
  • PMID: 18843642
  •     112 References
  •     42 citations


Background: Granulopoiesis-stimulating factors, such as granulocyte-colony-stimulating factor (G-CSF) and granulocyte-macrophage-colony-stimulating factor (GM-CSF), are being used to prevent febrile neutropenia and infection in patients undergoing treatment for malignant lymphoma. The question of whether G-CSF and GM-CSF improve dose intensity, tumour response, and overall survival in this patient population has not been answered yet. Since the results from single studies are inconclusive, a systematic review was undertaken.

Objectives: To determine the effectiveness of G-CSF and GM-CSF in patients with malignant lymphoma with respect to preventing neutropenia, febrile neutropenia and infection; improving quality of life, adherence to treatment protocol, tumour response, freedom from treatment failure (FFTF) and overall survival (OS); and adverse effects.

Search Strategy: We searched The Cochrane Library, MEDLINE, EMBASE, CancerLit, and other relevant literature databases; Internet databases of ongoing trials; and conference proceedings of the American Society of Clinical Oncology and the American Society of Hematology (1980 - 2007). We included full-text and abstract publications as well as unpublished data.

Selection Criteria: Randomised controlled trials comparing prophylaxis with G-CSF or GM-CSF versus placebo/no prophylaxis in adult patients with malignant lymphoma undergoing chemotherapy were included for review. Both study arms had to receive identical chemotherapy and supportive care.

Data Collection And Analysis: Trial eligibility and quality assessment, data extraction and analysis were done by two reviewers independently. Authors were contacted to obtain missing data.

Main Results: We included 13 eligible randomised controlled trials with 2607 randomised patients. Compared with no prophylaxis, both G-CSF and GM-CSF did not improve overall survival (hazard ratio 0.97; 95% CI 0.87 to 1.09) or FFTF (hazard ratio 1.11; 95% CI 0.91 to 1.35). Prophylaxis significantly reduced the relative risk (RR) for severe neutropenia (RR 0.67; 95% confidence interval (CI) 0.60 to 0.73), febrile neutropenia (RR 0.74; 95% CI 0.62 to 0.89) and infection (RR 0.74; 95% CI 0.64 to 0.85). There was no evidence that either G-CSF or GM-CSF reduced the number of patients requiring intravenous antibiotics (RR 0.82; 95%CI 0.57 to 1.18); lowered infection related mortality (RR 0.93; 95% CI 0.51 to 1.71); or improved complete tumour response (RR 1.03; 95% CI 0.95 to 1.10).One study evaluated quality of life parameters and found no differences between the treatment groups.

Authors' Conclusions: G-CSF and GM-CSF, when used as a prophylaxis in patients with malignant lymphoma undergoing conventional chemotherapy, reduce the risk of neutropenia, febrile neutropenia and infection. However, based on the randomised trials currently available, there is no evidence that either G-CSF or GM-CSF provide a significant advantage in terms of complete tumour response, FFTF or OS.

Use of granulocyte colony-stimulating factor (G-CSF) in patients receiving myelosuppressive chemotherapy for the treatment of cancer. Provincial Systemic Treatment Disease Site Group.
J Rusthoven, V Bramwell, B Stephenson.
Cancer Prev Control, 1999 Mar 27; 2(4). PMID: 10093631
MOPP/ABV/CAD chemotherapy with and without recombinant human granulocyte-macrophage colony stimulating factor in untreated, unfavorable prognosis Hodgkin's disease.
A Riccardi, P Gobbi, +5 authors, E Ascari.
Haematologica, 1993 Jan 01; 78(1). PMID: 7684012
CODE chemotherapy with and without granulocyte colony-stimulating factor in small-cell lung cancer.
M Fukuoka, N Masuda, +10 authors, K Furuse.
Br J Cancer, 1997 Jan 01; 75(2). PMID: 9010043    Free PMC article.
Phase II and dose-escalation with or without granulocyte colony-stimulating factor study of 9-aminocamptothecin in relapsed and refractory lymphomas.
W H Wilson, R Little, +6 authors, P Elwood.
J Clin Oncol, 1998 Jul 17; 16(7). PMID: 9667249
GM-CSF: clinical trials in non-Hodgkin's lymphoma patients with chemotherapy induced leucopenia.
A M Liberati, S Cinieri, +3 authors, F Grignani.
Leukemia, 1991 Jan 01; 5 Suppl 1. PMID: 1890860
G-CSF (filgrastim) as an adjunct to MOPP/ABVD therapy in Hodgkin's disease.
A Gustavsson.
Acta Oncol, 1997 Jan 01; 36(5). PMID: 9292744
[Usefulness of COP-BLAM therapy with concomitant G-CSF in elderly patients with non-Hodgkin's lymphoma in comparison with patients not given G-CSF].
N Niitsu, M Umeda.
Nihon Ronen Igakkai Zasshi, 1995 Jun 01; 32(6). PMID: 7563935
Comparison of pegfilgrastim with filgrastim on febrile neutropenia, grade IV neutropenia and bone pain: a meta-analysis of randomized controlled trials.
Lionel Pinto, Zhimei Liu, +3 authors, Gary Lyman.
Curr Med Res Opin, 2007 Aug 19; 23(9). PMID: 17697451
Quantitative relationships between circulating leukocytes and infection in patients with acute leukemia.
G P Bodey, M Buckley, Y S Sathe, E J Freireich.
Ann Intern Med, 1966 Feb 01; 64(2). PMID: 5216294
Highly Cited.
Efficacy of recombinant human granulocyte colony-stimulating factor and recombinant human granulocyte-macrophage colony-stimulating factor in neutropenic children with malignancies.
E Lydaki, E Bolonaki, +3 authors, M Kalmanti.
Pediatr Hematol Oncol, 1995 Nov 01; 12(6). PMID: 8589000
A comparison of efficacy of sargramostim (yeast-derived RhuGM-CSF) and filgrastim (bacteria-derived RhuG-CSF) in the therapeutic setting of chemotherapy-induced myelosuppression.
R A Beveridge, J A Miller, +22 authors, M J Sheridan.
Cancer Invest, 1998 Jul 29; 16(6). PMID: 9679526
Impact of primary prophylaxis with granulocyte colony-stimulating factor on febrile neutropenia and mortality in adult cancer patients receiving chemotherapy: a systematic review.
Nicole M Kuderer, David C Dale, Jeffrey Crawford, Gary H Lyman.
J Clin Oncol, 2007 Jul 20; 25(21). PMID: 17634496
Highly Cited. Systematic Review.
Recombinant human granulocyte-macrophage colony-stimulating factor accelerates neutrophil and monocyte recovery after allogeneic T-cell-depleted bone marrow transplantation.
T De Witte, A Gratwohl, +7 authors, W E Fibbe.
Blood, 1992 Mar 01; 79(5). PMID: 1536959
Randomized open label phase III trial of CEOP/IMVP-Dexa alternating chemotherapy and filgrastim versus CEOP/IMVP-Dexa alternating chemotherapy for aggressive non-Hodgkin's lymphoma (NHL). A multicenter trial by the Austrian Working Group for Medical Tumor Therapy.
M A Fridrik, R Greil, +11 authors, T Radaszkiewicz.
Ann Hematol, 1997 Dec 24; 75(4). PMID: 9402845
The importance of dose intensity in chemotherapy of metastatic breast cancer.
W Hryniuk, H Bush.
J Clin Oncol, 1984 Nov 01; 2(11). PMID: 6387060
Highly Cited. Review.
Are prophylactic haematopoietic growth factors of value in the management of patients with aggressive non-Hodgkin's lymphoma?
A Hackshaw, J Sweetenham, A Knight.
Br J Cancer, 2004 Apr 01; 90(7). PMID: 15054445    Free PMC article.
ICH Harmonised Tripartite Guideline. Statistical principles for clinical trials. International Conference on Harmonisation E9 Expert Working Group.
Stat Med, 1999 Oct 26; 18(15). PMID: 10532877
Highly Cited.
2006 update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline.
Thomas J Smith, James Khatcheressian, +19 authors, Antonio C Wolff.
J Clin Oncol, 2006 May 10; 24(19). PMID: 16682719
Highly Cited.
Randomized placebo-controlled trial of granulocyte-macrophage colony-stimulating factor in patients with chemotherapy-related febrile neutropenia.
E Vellenga, C A Uyl-de Groot, +10 authors, E G de Vries.
J Clin Oncol, 1996 Feb 01; 14(2). PMID: 8636779
Neutrophil recovery time and adverse side effects in acute leukemia patients treated with intensive chemotherapy and concomitant G or GM-CSF.
M L Alvarado Ibarra, J R Borbolla Escoboza, +4 authors, I Anaya Cuellar.
Rev Invest Clin, 1999 Jul 20; 51(2). PMID: 10410585
In vitro and in vivo analysis of the effects of recombinant human granulocyte colony-stimulating factor in patients.
M H Bronchud, M R Potter, +7 authors, N G Testa.
Br J Cancer, 1988 Jul 01; 58(1). PMID: 2458748    Free PMC article.
Filgrastim in patients with chemotherapy-induced febrile neutropenia. A double-blind, placebo-controlled trial.
D W Maher, G J Lieschke, +16 authors, G Morstyn.
Ann Intern Med, 1994 Oct 01; 121(7). PMID: 7520676
Risk assessment in cancer patients with fever and neutropenia: a prospective, two-center validation of a prediction rule.
J A Talcott, R D Siegel, R Finberg, L Goldman.
J Clin Oncol, 1992 Feb 01; 10(2). PMID: 1732432
Highly Cited.
[Clinical evaluation of rhG-CSF in patients with neutropenia induced by chemotherapy for multiple myeloma].
A Togawa, H Mizoguchi, +3 authors, F Takaku.
Rinsho Ketsueki, 2000 Mar 21; 41(2). PMID: 10723240
Infection risk and cancer chemotherapy: the impact of the chemotherapeutic regimen in patients with lymphoma and solid tissue malignancies.
E J Bow.
J Antimicrob Chemother, 1998 Aug 04; 41 Suppl D. PMID: 9688446
Recombinant granulocyte colony stimulating factor reduces the infectious complications of cytotoxic chemotherapy.
V Trillet-Lenoir, J Green, +7 authors, D Tomita.
Eur J Cancer, 1993 Jan 01; 29A(3). PMID: 7691119
Highly Cited.
Short-term rhG-CSF priming before chemotherapy does mobilize blood progenitors but does not prevent chemotherapy induced myelotoxicity: a randomized study of patients with non-Hodgkin's lymphomas.
P B Hansen, H E Johnsen, +3 authors, N E Hansen.
Leuk Lymphoma, 1995 Nov 01; 19(5-6). PMID: 8590846
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.
Michael Pfreundschuh, Lorenz Trümper, +12 authors, German High-Grade Non-Hodgkin's Lymphoma Study Group.
Blood, 2004 Feb 26; 104(3). PMID: 14982884
Assessing the quality of reports of randomized clinical trials: is blinding necessary?
A R Jadad, R A Moore, +4 authors, H J McQuay.
Control Clin Trials, 1996 Feb 01; 17(1). PMID: 8721797
Highly Cited.
Granulocyte colony-stimulating factor to prevent dose-limiting neutropenia in non-Hodgkin's lymphoma: a randomized controlled trial.
R Pettengell, H Gurney, +6 authors, D Crowther.
Blood, 1992 Sep 15; 80(6). PMID: 1381626
Effect of recombinant human granulocyte-macrophage colony-stimulating factor in patients with Hodgkin's disease: a phase I/II study.
D J Hovgaard, N I Nissen.
J Clin Oncol, 1992 Mar 01; 10(3). PMID: 1740678
Reduction by granulocyte colony-stimulating factor of fever and neutropenia induced by chemotherapy in patients with small-cell lung cancer.
J Crawford, H Ozer, +7 authors, G Rausch.
N Engl J Med, 1991 Jul 18; 325(3). PMID: 1711156
Highly Cited.
Human hematopoietic growth factors: old lessons and new perspectives.
W Dempke, A Von Poblozki, A Grothey, H J Schmoll.
Anticancer Res, 2001 May 01; 20(6D). PMID: 11326688
Recombinant human granulocyte-macrophage colony-stimulating factor after combined chemotherapy in high-grade non-Hodgkin's lymphoma--a randomised pilot study.
L Bergmann, T Karakas, +3 authors, D Hoelzer.
Eur J Cancer, 1995 Dec 01; 31A(13-14). PMID: 8652236
Recombinant human granulocyte-macrophage colony-stimulating factor reduces hematologic toxicity and widens clinical applicability of high-dose cyclophosphamide treatment in breast cancer and non-Hodgkin's lymphoma.
A M Gianni, M Bregni, +4 authors, G Bonadonna.
J Clin Oncol, 1990 May 01; 8(5). PMID: 2185337
A phase II trial of 200% ProMACE-CytaBOM in patients with previously untreated aggressive lymphomas: analysis of response, toxicity, and dose intensity.
L I Gordon, M Young, +6 authors, P A Cassileth.
Blood, 1999 Nov 24; 94(10). PMID: 10552939
Transplantation potential of hematopoietic cells released into the circulation during routine chemotherapy for non-Hodgkin's lymphoma.
R Pettengell, N G Testa, +2 authors, T M Dexter.
Blood, 1993 Oct 01; 82(7). PMID: 7691253
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.
Michael Pfreundschuh, Lorenz Trümper, +11 authors, German High-Grade Non-Hodgkin's Lymphoma Study Group.
Blood, 2004 Mar 16; 104(3). PMID: 15016643
Highly Cited.
Outline of clinical studies on recombinant human granulocyte colony stimulating factor (KRN 8601) in Japan.
T Kaneko, F Takaku, M Ogawa.
Tokai J Exp Clin Med, 1991 Mar 01; 16(1). PMID: 1723550
Prevention of chemotherapy-induced febrile neutropenia by prophylactic antibiotics plus or minus granulocyte colony-stimulating factor in small-cell lung cancer: a Dutch Randomized Phase III Study.
Johanna N Timmer-Bonte, Theo M de Boo, +9 authors, Vivianne C Tjan-Heijnen.
J Clin Oncol, 2005 Nov 01; 23(31). PMID: 16258098
Treatment of non-Hodgkin's lymphoma.
J O Armitage.
N Engl J Med, 1993 Apr 08; 328(14). PMID: 8450856
Clinical and virologic effects of recombinant human granulocyte-macrophage colony-stimulating factor in patients receiving chemotherapy for human immunodeficiency virus-associated non-Hodgkin's lymphoma: results of a randomized trial.
L D Kaplan, J O Kahn, +7 authors, P A Volberding.
J Clin Oncol, 1991 Jun 01; 9(6). PMID: 2033429
CHOP compared with CHOP plus granulocyte colony-stimulating factor in elderly patients with aggressive non-Hodgkin's lymphoma.
J K Doorduijn, B van der Holt, +13 authors, P Sonneveld.
J Clin Oncol, 2003 Aug 14; 21(16). PMID: 12915593
Effect of topical oral G-CSF on oral mucositis: a randomised placebo-controlled trial.
M Karthaus, C Rosenthal, +8 authors, A Ganser.
Bone Marrow Transplant, 1998 Nov 25; 22(8). PMID: 9827976
Meta-analysis: effect of prophylactic hematopoietic colony-stimulating factors on mortality and outcomes of infection.
Lillian Sung, Paul C Nathan, +2 authors, Joseph Beyene.
Ann Intern Med, 2007 Sep 19; 147(6). PMID: 17876022
A phase III trial comparing CHOP to PMitCEBO with or without G-CSF in patients aged 60 plus with aggressive non-Hodgkin's lymphoma.
C Burton, D Linch, +10 authors, D Cunningham.
Br J Cancer, 2006 Mar 02; 94(6). PMID: 16508640    Free PMC article.
Randomized multicentre trial of filgrastim as an adjunct to combination chemotherapy for Hodgkin's disease. West of Scotland Lymphoma Group.
D J Dunlop, M M Eatock, +7 authors, W P Steward.
Clin Oncol (R Coll Radiol), 1998 Jun 04; 10(2). PMID: 9610900
Efficacy of lenograstim on hematologic tolerance to MAID chemotherapy in patients with advanced soft tissue sarcoma and consequences on treatment dose-intensity.
B N Bui, B Chevallier, +7 authors, F Bonichon.
J Clin Oncol, 1995 Oct 01; 13(10). PMID: 7595717
The treatment of elderly patients with aggressive non-Hodgkin's lymphomas: feasibility and efficacy of an intensive multidrug regimen.
M Bertini, R Freilone, +11 authors, L Resegotti.
Leuk Lymphoma, 1996 Aug 01; 22(5-6). PMID: 8882962
Effect of granulocyte colony-stimulating factor on neutropenia due to chemotherapy for non-Hodgkin's lymphoma.
T Yoshida, S Nakamura, +7 authors, M Kanai.
Cancer, 1990 Nov 01; 66(9). PMID: 1699654
Sequential studies on the role of mitoxantrone, high-dose cytarabine, and recombinant human granulocyte-macrophage colony-stimulating factor in the treatment of refractory non-Hodgkin's lymphoma.
A D Ho, F Del Valle, +7 authors, W Fiedler.
Semin Oncol, 1990 Dec 01; 17(6 Suppl 10). PMID: 2259918
The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus.
A P Verhagen, H C de Vet, +4 authors, P G Knipschild.
J Clin Epidemiol, 1999 Mar 23; 51(12). PMID: 10086815
Highly Cited.
Quantitative model for multiple levels of drug resistance in clinical tumors.
J H Goldie, A J Coldman.
Cancer Treat Rep, 1983 Oct 01; 67(10). PMID: 6627236
Role of granulocyte colony-stimulating factor in relapsed/resistant intermediate and high-grade non-Hodgkin's lymphoma patients treated with the E-SHAP regimen.
M Mangiagalli, I Miccolis, +2 authors, G Corneo.
Tumori, 1995 Mar 01; 81(2). PMID: 7539966
The combination of fludarabine, cyclophosphamide, and granulocyte-macrophage colony-stimulating factor in the treatment of patients with relapsed chronic lymphocytic leukemia and low-grade Non-Hodgkin's lymphoma.
Ruta Rao, Jamile M Shammo, +4 authors, Stephanie A Gregory.
Clin Lymphoma, 2005 Jul 02; 6(1). PMID: 15989703
Effect of granulocyte colony-stimulating factor in patients with diffuse large cell lymphoma treated with intensive chemotherapy.
A Avilés, J C Díaz-Maqueo, +2 authors, E L García.
Leuk Lymphoma, 1994 Sep 01; 15(1-2). PMID: 7532056
Economic analysis of lenograstim in the correction of neutropenia following chemotherapy for non-Hodgkin's lymphoma.
E Souêtre, W Qing.
Pharmacoeconomics, 1993 Dec 09; 6 Suppl 2. PMID: 10172484
Cost analyses of adjunct colony stimulating factors for acute leukemia: can they improve clinical decision making.
C L Bennett, T J Stinson, +3 authors, M S Tallman.
Leuk Lymphoma, 2000 Mar 18; 37(1-2). PMID: 10721770
Thrombosis in cancer patients treated with hematopoietic growth factors--a meta-analysis. On behalf of the Subcommittee on Haemostasis and Malignancy of the Scientific and Standardization Committee of the ISTH.
T Barbui, G Finazzi, A Grassi, R Marchioli.
Thromb Haemost, 1996 Feb 01; 75(2). PMID: 8815592
A cost analysis of hematopoietic colony-stimulating factors.
G H Lyman, L Balducci.
Oncology (Williston Park), 1995 Nov 01; 9(11 Suppl). PMID: 8608061
The chemotherapy of lymphomas: looking back, moving forward--the Richard and Hinda Rosenthal Foundation award lecture.
V T De Vita, S M Hubbard, D L Longo.
Cancer Res, 1987 Nov 15; 47(22). PMID: 3311358
Randomized comparison between antibiotics alone and antibiotics plus granulocyte-macrophage colony-stimulating factor (Escherichia coli-derived in cancer patients with fever and neutropenia.
E J Anaissie, S Vartivarian, +5 authors, S Vadhan-Raj.
Am J Med, 1996 Jan 01; 100(1). PMID: 8579082
Granulocyte colony-stimulating factor in severe chemotherapy-induced afebrile neutropenia.
L C Hartmann, L K Tschetter, +9 authors, C G Moertel.
N Engl J Med, 1997 Jun 19; 336(25). PMID: 9187067
Shortened time to recovery from chemotherapy induced neutropenia in pediatric patients with high dose combined cytokines.
G Deb, A Donfrancesco, +4 authors, L Helson.
Anticancer Res, 1998 May 06; 18(1B). PMID: 9568167
Update of recommendations for the use of hematopoietic colony-stimulating factors: evidence-based clinical practice guidelines. American Society of Clinical Oncology.
J Clin Oncol, 1996 Jun 01; 14(6). PMID: 8656266
Cytokine efficiency in the treatment of high-grade malignant non-Hodgkin's lymphomas: results of a randomized double-blind placebo-controlled study with intensified COP-BLAM +/- rhGM-CSF.
M Engelhard, H Gerhartz, +7 authors, D Huhn.
Ann Oncol, 1994 Jan 01; 5 Suppl 2. PMID: 7515644
Dose intensity versus total dose of chemotherapy: an experimental basis.
H E Skipper.
Important Adv Oncol, 1990 Jan 01;. PMID: 2182523
Recombinant human granulocyte-macrophage colony-stimulating factor (rhGM-CSF) after chemotherapy in patients with non-Hodgkin's lymphoma; a placebo-controlled double blind phase III trial.
K Kaku, M Takahashi, +6 authors, S Miwa.
Leuk Lymphoma, 1993 Oct 01; 11(3-4). PMID: 8260897
Bias in meta-analysis detected by a simple, graphical test.
M Egger, G Davey Smith, M Schneider, C Minder.
BMJ, 1997 Oct 06; 315(7109). PMID: 9310563    Free PMC article.
Highly Cited.
Can cytotoxic dose-intensity be increased by using granulocyte colony-stimulating factor? A randomized controlled trial of lenograstim in small-cell lung cancer.
P J Woll, J Hodgetts, +3 authors, N Thatcher.
J Clin Oncol, 1995 Mar 01; 13(3). PMID: 7533825
The Multinational Association for Supportive Care in Cancer risk index: A multinational scoring system for identifying low-risk febrile neutropenic cancer patients.
J Klastersky, M Paesmans, +8 authors, J Talcott.
J Clin Oncol, 2000 Aug 16; 18(16). PMID: 10944139
Highly Cited.
Adults and children with small non-cleaved-cell lymphoma have a similar excellent outcome when treated with the same chemotherapy regimen.
I Magrath, M Adde, +9 authors, I D Horak.
J Clin Oncol, 1996 Mar 01; 14(3). PMID: 8622041
Granulocyte colony-stimulating factor (G-CSF) with or without a quinolone in the prevention of infection in cancer patients.
A G Maiche, T Muhonen.
Eur J Cancer, 1993 Jan 01; 29A(10). PMID: 7691114
Elderly aggressive-histology non-Hodgkin's lymphoma: first-line VNCOP-B regimen experience on 350 patients.
P L Zinzani, S Storti, +20 authors, S Tura.
Blood, 1999 Jun 25; 94(1). PMID: 10381495
Randomized trial with or without granulocyte colony-stimulating factor as adjunct to induction VNCOP-B treatment of elderly high-grade non-Hodgkin's lymphoma.
P L Zinzani, E Pavone, +16 authors, S Tura.
Blood, 1997 Jun 01; 89(11). PMID: 9166835
A predictive model for neutropenia associated with cancer chemotherapy.
G H Lyman.
Pharmacotherapy, 2000 Jul 25; 20(7 Pt 2). PMID: 10905685
Standard and increased-dose BEACOPP chemotherapy compared with COPP-ABVD for advanced Hodgkin's disease.
Volker Diehl, Jeremy Franklin, +10 authors, German Hodgkin's Lymphoma Study Group.
N Engl J Med, 2003 Jun 13; 348(24). PMID: 12802024
Highly Cited.
A single-blind, randomised, vehicle-controlled dose-finding study of recombinant human granulocyte colony-stimulating factor (lenograstim) in patients undergoing chemotherapy for solid cancers and lymphoma.
A M Seymour, E de Campos, +7 authors, W E Berdel.
Eur J Cancer, 1995 Dec 01; 31A(13-14). PMID: 8652235
Effect of granulocyte colony stimulating factor on neutropenia induced by cytotoxic chemotherapy.
G Morstyn, L Campbell, +6 authors, R Fox.
Lancet, 1988 Mar 26; 1(8587). PMID: 2895212
Highly Cited.
CHOP is superior to CNOP in elderly patients with aggressive lymphoma while outcome is unaffected by filgrastim treatment: results of a Nordic Lymphoma Group randomized trial.
Eva Osby, Hans Hagberg, +8 authors, Nordic Lymphoma Group.
Blood, 2003 Jan 18; 101(10). PMID: 12531794
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.
H Ozer, J O Armitage, +12 authors, American Society of Clinical Oncology.
J Clin Oncol, 2000 Oct 14; 18(20). PMID: 11032599
Additional chemotherapy agents improve treatment outcome for children and adults with advanced B-cell lymphomas.
M Adde, A Shad, +9 authors, I Magrath.
Semin Oncol, 1998 May 13; 25(2 Suppl 4). PMID: 9578060
Prognostic significance of received relative dose intensity in non-Hodgkin's lymphoma patients: application to LNH-87 protocol. The GELA. (Groupe d'Etude des Lymphomes de l'Adulte).
E Lepage, C Gisselbrecht, +7 authors, B Coiffier.
Ann Oncol, 1993 Sep 01; 4(8). PMID: 7694634
Cost-benefit of granulocyte colony-stimulating factor administration in older patients with non-Hodgkin's lymphoma treated with combination chemotherapy.
V Zagonel, R Babare, +5 authors, S Monfardini.
Ann Oncol, 1994 Jan 01; 5 Suppl 2. PMID: 7515645
Protective effect of partially purified human urinary colony-stimulating factor on granulocytopenia after antitumor chemotherapy.
K Motoyoshi, F Takaku, +7 authors, M Ogawa.
Exp Hematol, 1986 Dec 01; 14(11). PMID: 3490992
Short term treatment with Escherichia coli recombinant human granulocyte-macrophage-colony stimulating factor prior to chemotherapy for Hodgkin disease.
M Aglietta, F Montemurro, +10 authors, A Levis.
Cancer, 2000 Jan 21; 88(2). PMID: 10640980
[Granulocyte colony-stimulating factor in the treatment of febrile neutropenia].
M A López-Hernández, R Jiménez-Alvarado, +5 authors, I Anaya-Cuéllar.
Gac Med Mex, 2000 May 18; 136(2). PMID: 10815320
Prophylactic granulocyte colony-stimulating factor in patients receiving dose-intensive cancer chemotherapy: a meta-analysis.
Gary H Lyman, Nicole M Kuderer, Benjamin Djulbegovic.
Am J Med, 2002 Mar 21; 112(5). PMID: 11904116
Randomized, double-blind, placebo-controlled, phase III study of recombinant human granulocyte-macrophage colony-stimulating factor as adjunct to induction treatment of high-grade malignant non-Hodgkin's lymphomas.
H H Gerhartz, M Engelhard, +7 authors, W Siegert.
Blood, 1993 Oct 15; 82(8). PMID: 7691256
Average relative dose intensity and the impact on design of clinical trials.
W M Hryniuk.
Semin Oncol, 1987 Mar 01; 14(1). PMID: 3823917
American Society of Clinical Oncology. Recommendations for the use of hematopoietic colony-stimulating factors: evidence-based, clinical practice guidelines.
J Clin Oncol, 1994 Nov 01; 12(11). PMID: 7964965
Recombinant human granulocyte-macrophage colony-stimulating factor stimulates in vitro mature human neutrophil and eosinophil function, surface receptor expression, and survival.
A F Lopez, D J Williamson, +7 authors, M A Vadas.
J Clin Invest, 1986 Nov 01; 78(5). PMID: 3021817    Free PMC article.
Highly Cited.
Dose intensity of standard adjuvant CMF with granulocyte colony-stimulating factor for premenopausal patients with node-positive breast cancer.
H de Graaf, P H Willemse, +5 authors, E G de Vries.
Oncology, 1996 Jul 01; 53(4). PMID: 8692532
Identifying relevant studies for systematic reviews.
K Dickersin, R Scherer, C Lefebvre.
BMJ, 1994 Nov 12; 309(6964). PMID: 7718048    Free PMC article.
Highly Cited. Systematic Review.
Recombinant human granulocyte-macrophage colony-stimulating factor as adjunct to chemotherapy in aggressive non-Hodgkin's lymphomas.
H H Gerhartz, M Engelhard, +7 authors, A C Stern.
Semin Oncol, 1994 Dec 01; 21(6 Suppl 16). PMID: 7528447
Infection in cancer patients. A continuing association.
G P Bodey.
Am J Med, 1986 Jul 28; 81(1A). PMID: 3526877
Highly Cited. Review.
Improving treatment of chemotherapy-induced neutropenic fever by administration of colony-stimulating factors.
J I Mayordomo, F Rivera, +7 authors, I García-Ribas.
J Natl Cancer Inst, 1995 Jun 07; 87(11). PMID: 7540696
Randomized placebo-controlled trial of granulocyte-macrophage colony-stimulating-factor support for dose-intensive cyclophosphamide, etoposide, and cisplatin.
J C Yau, J A Neidhart, +7 authors, J Holcenberg.
Am J Hematol, 1996 Apr 01; 51(4). PMID: 8602629
Intervention treatment of established neutropenia with human recombinant granulocyte-macrophage colony-stimulating factor (rhGM-CSF) in patients undergoing cancer chemotherapy.
H H Gerhartz, A C Stern, +5 authors, W Wilmanns.
Leuk Res, 1993 Feb 01; 17(2). PMID: 8429694
[Clinical study of recombinant human granulocyte-macrophage colony-stimulating factor on chemotherapy-induced leukopenia].
Y K Shi, Y Sun, M Su.
Zhonghua Zhong Liu Za Zhi, 1994 Sep 01; 16(5). PMID: 7895587
Role of granulocyte-macrophage colony-stimulating factor as adjuvant treatment in neutropenic patients with bacterial and fungal infection.
G P Bodey, E Anaissie, J Gutterman, S Vadhan-Raj.
Eur J Clin Microbiol Infect Dis, 1994 Jan 01; 13 Suppl 2. PMID: 7875147
Analysis of dose intensity for adjuvant chemotherapy trials in stage II breast cancer.
W Hryniuk, M N Levine.
J Clin Oncol, 1986 Aug 01; 4(8). PMID: 3525765
Highly Cited.
Effect of granulocyte-colony stimulating factor on empiric therapy with flomoxef sodium and tobramycin in febrile neutropenic patients with hematological malignancies. Kan-etsu Hematological Disease and Infection Study Group.
M Yoshida, M Karasawa, +12 authors, Y Miura.
Int J Hematol, 1999 Mar 11; 69(2). PMID: 10071455
Impact of granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF in patients with malignant lymphoma: a systematic review.
Julia Bohlius, Marcel Reiser, Guido Schwarzer, Andreas Engert.
Br J Haematol, 2003 Jul 25; 122(3). PMID: 12877668
Systematic Review.
Lenograstim prevents morbidity from intensive induction chemotherapy in the treatment of inflammatory breast cancer.
B Chevallier, P Chollet, +7 authors, C Fizames.
J Clin Oncol, 1995 Jul 01; 13(7). PMID: 7541448
Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints.
M K Parmar, V Torri, L Stewart.
Stat Med, 1999 Jan 28; 17(24). PMID: 9921604
Highly Cited.
[A phase III study of KRN 8601 (rhG-CSF) on neutropenia induced by chemotherapy for malignant lymphoma--a multi-institutional placebo controlled double-blind comparative study].
M Ogawa, T Masaoka, +2 authors, M Nakashima.
Gan To Kagaku Ryoho, 1990 Mar 01; 17(3 Pt 1). PMID: 1689988
Economic impact of granulopoiesis stimulating agents on the management of febrile neutropenia.
G H Lyman, N M Kuderer, L Balducci.
Curr Opin Oncol, 1998 Aug 14; 10(4). PMID: 9702395
Prospective randomized placebo-controlled study of granulocyte-macrophage colony-stimulating factor without stem-cell transplantation after high-dose melphalan in patients with multiple myeloma.
P Moreau, D Fiere, +9 authors, J L Harousseau.
J Clin Oncol, 1997 Feb 01; 15(2). PMID: 9053491
EORTC guidelines for the use of granulocyte-colony stimulating factor to reduce the incidence of chemotherapy-induced febrile neutropenia in adult patients with lymphomas and solid tumours.
M S Aapro, D A Cameron, +10 authors, European Organisation for Research and Treatment of Cancer (EORTC) Granulocyte Colony-Stimulating Factor (G-CSF) Guidelines Working Party.
Eur J Cancer, 2006 Jun 06; 42(15). PMID: 16750358
Highly Cited. Systematic Review.
Neutropenic complications in advanced-stage non-Hodgkin's lymphoma: implications for the use of prophylactic recombinant human granulocyte-colony stimulating factor (G-CSF).
N Bobey, R C Woodman.
Clin Invest Med, 1998 May 01; 21(2). PMID: 9562926
Placebo-controlled phase III study of lenograstim (glycosylated recombinant human granulocyte colony-stimulating factor) in aggressive non-Hodgkin's lymphoma: factors influencing chemotherapy administration. Groupe d'Etude des Lymphomes de l'Adulte.
C Gisselbrecht, C Haioun, +12 authors, F Reyes.
Leuk Lymphoma, 1997 Apr 01; 25(3-4). PMID: 9168439
Advances in the treatment of neutropenia.
David C Dale.
Curr Opin Support Palliat Care, 2009 Jun 25; 3(3). PMID: 19550332    Free PMC article.
Implications of the European Organisation for Research And Treatment Of Cancer (EORTC) guidelines on the use of granulocyte colony-stimulating factor (G-CSF) for lymphoma care.
Ruth Pettengell, Matti Aapro, +5 authors, Jan Walewski.
Clin Drug Investig, 2009 Jul 14; 29(8). PMID: 19591512
Prophylaxis of chemotherapy-induced febrile neutropenia with granulocyte colony-stimulating factors: where are we now?
Matti Aapro, Jeffrey Crawford, Didier Kamioner.
Support Care Cancer, 2010 Mar 02; 18(5). PMID: 20191292    Free PMC article.
Non-Hodgkin's lymphoma in the elderly.
Paolo F Caimi, Paul M Barr, Nathan A Berger, Hillard M Lazarus.
Drugs Aging, 2010 Mar 10; 27(3). PMID: 20210368
Pharmacokinetic profiles of a biosimilar filgrastim and Amgen filgrastim: results from a randomized, phase I trial.
Cornelius F Waller, Miguel Bronchud, Stuart Mair, Rodeina Challand.
Ann Hematol, 2010 Apr 30; 89(9). PMID: 20428872    Free PMC article.
Bending the cost curve in cancer care.
Thomas J Smith, Bruce E Hillner.
N Engl J Med, 2011 May 27; 364(21). PMID: 21612477    Free PMC article.
Highly Cited.
Neutropenia and Neutropenic Complications in ABVD Chemotherapy for Hodgkin Lymphoma.
Bhanu Vakkalanka, Brian K Link.
Adv Hematol, 2011 Jun 21; 2011. PMID: 21687649    Free PMC article.
Febrile neutropenia in adjuvant docetaxel and cyclophosphamide (TC) with prophylactic pegfilgrastim in breast cancer patients: a retrospective analysis.
Nuttapong Ngamphaiboon, Tracey L O'Connor, +2 authors, Ellen B Kossoff.
Med Oncol, 2011 Aug 06; 29(3). PMID: 21818673
Re: personalized medicine and cancer supportive care: appropriate use of colony-stimulating factor support of chemotherapy.
Arnold L Potosky, Jennifer L Malin, +2 authors, Jane C Weeks.
J Natl Cancer Inst, 2011 Nov 01; 103(24). PMID: 22036767    Free PMC article.
The glutathione disulfide mimetic NOV-002 inhibits cyclophosphamide-induced hematopoietic and immune suppression by reducing oxidative stress.
C Marcela Diaz-Montero, Yong Wang, +5 authors, Daohong Zhou.
Free Radic Biol Med, 2012 Feb 22; 52(9). PMID: 22343421    Free PMC article.
A way forward on the medically appropriate use of white cell growth factors.
Thomas J Smith, Bruce E Hillner.
J Clin Oncol, 2012 Mar 01; 30(14). PMID: 22370327    Free PMC article.
Pharmacoeconomics of the myeloid growth factors: a critical and systematic review.
Bradford R Hirsch, Gary H Lyman.
Pharmacoeconomics, 2012 May 01; 30(6). PMID: 22540394
Systematic Review.
SEOM clinical guidelines for myeloid growth factors.
José Muñoz Langa, Pere Gascón, Javier de Castro, SEOM (Spanish Society of Clinical Oncology).
Clin Transl Oncol, 2012 Jun 23; 14(7). PMID: 22721792
Primary prophylaxis with granulocyte colony-stimulating factor (GCSF) reduces the incidence of febrile neutropenia in patients with non-Hodgkin lymphoma (NHL) receiving CHOP chemotherapy treatment without adversely affecting their quality of life: cost-benefit and quality of life analysis.
Sophie Lee, Angela Knox, +3 authors, Samar Issa.
Support Care Cancer, 2012 Sep 14; 21(3). PMID: 22972488
Impact of dose intensity on outcome of fludarabine, cyclophosphamide, and rituximab regimen given in the first-line therapy for chronic lymphocytic leukemia.
Emmanuelle Bouvet, Cécile Borel, +5 authors, Loic Ysebaert.
Haematologica, 2012 Oct 16; 98(1). PMID: 23065520    Free PMC article.
Retinoid agonist Am80-enhanced neutrophil bactericidal activity arising from granulopoiesis in vitro and in a neutropenic mouse model.
Wanjing Ding, Hiroyuki Shimada, +6 authors, Lingtao Wu.
Blood, 2012 Dec 18; 121(6). PMID: 23243275    Free PMC article.
Colony-stimulating factors for febrile neutropenia during cancer therapy.
Charles L Bennett, Benjamin Djulbegovic, LeAnn B Norris, James O Armitage.
N Engl J Med, 2013 Mar 22; 368(12). PMID: 23514290    Free PMC article.
The MASCC Neutropenia, Infection and Myelosuppression Study Group evaluates recent new concepts for the use of granulocyte colony-stimulating factors for the prevention of febrile neutropenia.
Jean Klastersky, Harry Raftopoulos, Bernardo Rapoport.
Support Care Cancer, 2013 Mar 26; 21(6). PMID: 23525960
Fludarabine, cyclophosphamide and rituximab plus granulocyte macrophage colony-stimulating factor as frontline treatment for patients with chronic lymphocytic leukemia.
Paolo Strati, Alessandra Ferrajoli, +4 authors, Stefan Faderl.
Leuk Lymphoma, 2013 Jul 03; 55(4). PMID: 23808813    Free PMC article.
Primary prophylaxis with hematopoietic colony stimulating factor: insights from a Canadian cost-effectiveness analysis.
Scott A Strassels, Michael Dickson, Leann B Norris, Charles L Bennett.
J Natl Cancer Inst, 2013 Jul 23; 105(15). PMID: 23873406    Free PMC article.
Febrile neutropenia in hematologic malignancies.
Michael K Keng, Mikkael A Sekeres.
Curr Hematol Malig Rep, 2013 Aug 31; 8(4). PMID: 23990311
Granulocyte colony-stimulating factors as prophylaxis against febrile neutropenia.
Sol Cortés de Miguel, Miguel Ángel Calleja-Hernández, Salomón Menjón-Beltrán, Inmaculada Vallejo-Rodríguez.
Support Care Cancer, 2014 Oct 07; 23(2). PMID: 25284722
Comparison of Therapeutic G-CSF Cycles and Prophylactic G-CSF Cycles in Patients Receiving Paclitaxel and Carboplatin Combination Chemotherapy for Ovarian Cancer: A Retrospective Study Report.
Masaaki Kawashima, Hajime Kondo.
J Rural Med, 2015 Feb 05; 9(2). PMID: 25648659    Free PMC article.
Sepsis in standard care: patients' characteristics, effectiveness of antimicrobial therapy and patient outcome--a cohort study.
Franz Ratzinger, Katharina Eichbichler, +7 authors, Heinz Burgmann.
Infection, 2015 Apr 05; 43(3). PMID: 25840554
Colony-stimulating factors for chemotherapy-related febrile neutropenia are associated with improved prognosis in adult acute lymphoblastic leukemia.
Shi-Guang Ye, Y I Ding, +3 authors, Ai-Bin Liang.
Mol Clin Oncol, 2015 Jul 15; 3(3). PMID: 26161258    Free PMC article.
A Phase III Study of Balugrastim Versus Pegfilgrastim in Breast Cancer Patients Receiving Chemotherapy With Doxorubicin and Docetaxel.
Oleg Gladkov, Vladimir Moiseyenko, +4 authors, Noa Avisar.
Oncologist, 2015 Dec 17; 21(1). PMID: 26668251    Free PMC article.
Biosimilars in the management of neutropenia: focus on filgrastim.
Désirée Caselli, Simone Cesaro, Maurizio Aricò.
Biologics, 2016 Mar 05; 10. PMID: 26937170    Free PMC article.
Efficacy and safety of acupuncture for chemotherapy-induced leucopoenia: protocol for a systematic review.
Jiayun Nian, Xu Sun, +6 authors, Ganlin Zhang.
BMJ Open, 2016 May 28; 6(5). PMID: 27231002    Free PMC article.
Management of neutropenic patients in the intensive care unit (NEWBORNS EXCLUDED) recommendations from an expert panel from the French Intensive Care Society (SRLF) with the French Group for Pediatric Intensive Care Emergencies (GFRUP), the French Society of Anesthesia and Intensive Care (SFAR), the French Society of Hematology (SFH), the French Society for Hospital Hygiene (SF2H), and the French Infectious Diseases Society (SPILF).
David Schnell, Elie Azoulay, +17 authors, Michael Darmon.
Ann Intensive Care, 2016 Sep 18; 6(1). PMID: 27638133    Free PMC article.
Am80-GCSF synergizes myeloid expansion and differentiation to generate functional neutrophils that reduce neutropenia-associated infection and mortality.
Lin Li, Xiaotian Qi, +12 authors, Lingtao Wu.
EMBO Mol Med, 2016 Nov 04; 8(11). PMID: 27737899    Free PMC article.
The immune system's role in sepsis progression, resolution, and long-term outcome.
Matthew J Delano, Peter A Ward.
Immunol Rev, 2016 Oct 27; 274(1). PMID: 27782333    Free PMC article.
Highly Cited. Review.
Infection is an Independent Predictor of Death in Diffuse Large B Cell Lymphoma.
Claire Dendle, Michael Gilbertson, +5 authors, Zoe McQuilten.
Sci Rep, 2017 Jul 02; 7(1). PMID: 28667319    Free PMC article.
Clinical validation of genetic variants associated with in vitro chemotherapy-related lymphoblastoid cell toxicity.
Peter A Fasching, Lothar Häberle, +19 authors, Liewei Wang.
Oncotarget, 2017 Nov 05; 8(44). PMID: 29100455    Free PMC article.
Model-based optimization of G-CSF treatment during cytotoxic chemotherapy.
Sibylle Schirm, Christoph Engel, +2 authors, Markus Scholz.
J Cancer Res Clin Oncol, 2017 Nov 06; 144(2). PMID: 29103159    Free PMC article.
Strategies to generate functionally normal neutrophils to reduce infection and infection-related mortality in cancer chemotherapy.
Hisham Abdel-Azim, Weili Sun, Lingtao Wu.
Pharmacol Ther, 2019 Aug 31; 204. PMID: 31470030    Free PMC article.
A method to determine if more than surrogate outcomes were improved: The EMR glitch experiment.
Jennifer Gill, Vinay Prasad.
Res Pract Thromb Haemost, 2020 Jan 29; 4(1). PMID: 31989081    Free PMC article.
Targeting the host-pathogen interface for treatment of Staphylococcus aureus infection.
Bonggoo Park, George Y Liu.
Semin Immunopathol, 2011 Nov 18; 34(2). PMID: 22089960
Clinical utility of polyethylene glycol conjugated granulocyte colony-stimulating factor (PEG-G-CSF) for preventing severe neutropenia in metastatic colorectal cancer patients treated with FOLFOXIRI plus bevacizumab: a single-center retrospective study.
Yusuke Kitagawa, Hiroki Osumi, +10 authors, Kensei Yamaguchi.
BMC Cancer, 2020 Apr 30; 20(1). PMID: 32345249    Free PMC article.
Prophylactic antibiotics or G(M)-CSF for the prevention of infections and improvement of survival in cancer patients receiving myelotoxic chemotherapy.
Nicole Skoetz, Julia Bohlius, +3 authors, Jörg-Janne Vehreschild.
Cochrane Database Syst Rev, 2015 Dec 22; (12). PMID: 26687844    Free PMC article.
Systematic Review.
Comparative effectiveness of white blood cell growth factors on neutropenia, infection, and survival in older people with non-Hodgkin's lymphoma treated with chemotherapy.
Stephen K Gruschkus, David Lairson, +2 authors, Xianglin L Du.
J Am Geriatr Soc, 2010 Sep 16; 58(10). PMID: 20840455    Free PMC article.
Immune-Based Anti-Staphylococcal Therapeutic Approaches.
Bonggoo Park, George Y Liu.
Microorganisms, 2021 Feb 11; 9(2). PMID: 33562054    Free PMC article.
Effectiveness of Herbal Medicine for Leukopenia/Neutropenia Induced by Chemotherapy in Adults with Colorectal Cancer: A Systematic Review and Meta-analysis.
Shao-Hua Yan, Shuo Feng, +11 authors, Yu-Fei Yang.
Integr Cancer Ther, 2021 Jun 13; 20. PMID: 34116595    Free PMC article.