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Published in: Journal of Neuro-Oncology 1/2014

01-03-2014 | Clinical Study

Factors impacting survival following second surgery in patients with glioblastoma in the temozolomide treatment era, incorporating neutrophil/lymphocyte ratio and time to first progression

Authors: Mairéad G. McNamara, Zarnie Lwin, Haiyan Jiang, Arnoud J. Templeton, Gelareh Zadeh, Mark Bernstein, Caroline Chung, Barbara-Ann Millar, Normand Laperriere, Warren P. Mason

Published in: Journal of Neuro-Oncology | Issue 1/2014

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Abstract

Patients with progressive glioblastoma (GBM) have a poor prognosis. Neutrophil/lymphocyte ratio (NLR), a host inflammatory marker, is prognostic in several solid tumors. The prognostic impact of either NLR, or time from first surgery for GBM to first progression (TTP), in patients undergoing second surgery, has not been assessed. Patients undergoing second surgery for GBM were retrospectively reviewed. Primary outcome was overall survival (OS) and Cox proportional hazard models were used to assess the prognostic value of baseline characteristics including TTP and NLR. Univariable and multivariable analysis (MVA) of OS from second surgery were performed using accelerated failure time Weibull model. Of 584 patients with GBM, 107 (18 %) underwent second surgery between 01/04 and 12/11. Patients who underwent second surgery had longer OS versus those having primary surgery alone; 20.9 versus 9.9 months (P < 0.001). Median OS from second surgery in patients with NLR ≤ 4 versus NLR > 4 was 9.7 versus 5.9 months (log rank P = 0.02). The NLR retained its prognostic significance for survival on MVA (time ratio [TR] 1.65, 95 % confidence interval [CI] 1.15–2.35, P < 0.01). No chemotherapy post second surgery (TR 0.23, 95 % CI 0.16–0.33, P < 0.001) portended worse survival. In patients undergoing second surgery, when TTP was ≤12 months, 12–24 months, or >24 months, median OS from second surgery was 7.2, 7.0 and 6.3 months, respectively (P = 0.6). A NLR > 4 prior to second surgery is a poor prognostic factor in GBM and later progression is associated with longer survival in patients but not in longer survival after second surgery.
Literature
1.
go back to reference Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef
2.
go back to reference Ammirati M, Galicich JH, Arbit E, Liao Y (1987) Reoperation in the treatment of recurrent intracranial malignant gliomas. Neurosurgery 21:607–614PubMedCrossRef Ammirati M, Galicich JH, Arbit E, Liao Y (1987) Reoperation in the treatment of recurrent intracranial malignant gliomas. Neurosurgery 21:607–614PubMedCrossRef
3.
go back to reference Barker FG, Chang SM, Gutin PH et al (1998) Survival and functional status after resection of recurrent glioblastoma multiforme. Neurosurgery 42:709–720PubMedCrossRef Barker FG, Chang SM, Gutin PH et al (1998) Survival and functional status after resection of recurrent glioblastoma multiforme. Neurosurgery 42:709–720PubMedCrossRef
4.
go back to reference Dirks GR, Bernstein M, Muller PJ, Tucker WS (1993) The value of reoperation for recurrent glioblastoma. Can J Surg 36:271–275PubMed Dirks GR, Bernstein M, Muller PJ, Tucker WS (1993) The value of reoperation for recurrent glioblastoma. Can J Surg 36:271–275PubMed
5.
go back to reference Harsh GR, Levin VA, Gutin PH et al (1987) Reoperation for recurrent glioblastoma and anaplastic astrocytoma. Neurosurgery 21:615–621PubMedCrossRef Harsh GR, Levin VA, Gutin PH et al (1987) Reoperation for recurrent glioblastoma and anaplastic astrocytoma. Neurosurgery 21:615–621PubMedCrossRef
6.
go back to reference Proctor MJ, Morrison DS, Talwar D et al (2011) A comparison of inflammation-based prognostic scores in patients with cancer. A Glasgow inflammation outcome study. Eur J Cancer 47:2633–2641PubMedCrossRef Proctor MJ, Morrison DS, Talwar D et al (2011) A comparison of inflammation-based prognostic scores in patients with cancer. A Glasgow inflammation outcome study. Eur J Cancer 47:2633–2641PubMedCrossRef
7.
go back to reference Templeton AJ, McNamara MG, Vera-Badillo et al (2013) Prognostic role of neutrophil to lymphocyte ratio (nlr) in solid tumors: a systematic review and meta-analysis. Eur J Cancer 47: (Suppl 1, abstract 1008) Templeton AJ, McNamara MG, Vera-Badillo et al (2013) Prognostic role of neutrophil to lymphocyte ratio (nlr) in solid tumors: a systematic review and meta-analysis. Eur J Cancer 47: (Suppl 1, abstract 1008)
8.
go back to reference Guthrie GJ, Charles KA, Roxburgh CS, Horgan PG, McMillan DC, Clarke SJ (2013) The systemic inflammation-based neutrophil–lymphocyte ratio: experience in patients with cancer. Crit Rev Oncol Hematol 88:218–230PubMedCrossRef Guthrie GJ, Charles KA, Roxburgh CS, Horgan PG, McMillan DC, Clarke SJ (2013) The systemic inflammation-based neutrophil–lymphocyte ratio: experience in patients with cancer. Crit Rev Oncol Hematol 88:218–230PubMedCrossRef
9.
go back to reference Petrie HT, Klassen LW, Kay HD (1985) Inhibition of human cytotoxic T lymphocyte activity in vitro by autologous peripheral blood granulocytes. J Immunol 134:230–234PubMed Petrie HT, Klassen LW, Kay HD (1985) Inhibition of human cytotoxic T lymphocyte activity in vitro by autologous peripheral blood granulocytes. J Immunol 134:230–234PubMed
10.
go back to reference El-Hag A, Clark RA (1987) Immunosuppression by activated human neutrophils. Dependence on the myeloperoxidase system. J Immunol 139:2406–2413PubMed El-Hag A, Clark RA (1987) Immunosuppression by activated human neutrophils. Dependence on the myeloperoxidase system. J Immunol 139:2406–2413PubMed
11.
go back to reference McCourt M, Wang JH, Sookhai S, Redmond HP (1999) Proinflammatory mediators stimulate neutrophil-directed angiogenesis. Arch Surg 134:1325–1331PubMedCrossRef McCourt M, Wang JH, Sookhai S, Redmond HP (1999) Proinflammatory mediators stimulate neutrophil-directed angiogenesis. Arch Surg 134:1325–1331PubMedCrossRef
12.
go back to reference Di Carlo E, Forni G, Musiani P (2003) Neutrophils in the antitumoral immune response. Chem Immunol Allergy 83:182–203PubMedCrossRef Di Carlo E, Forni G, Musiani P (2003) Neutrophils in the antitumoral immune response. Chem Immunol Allergy 83:182–203PubMedCrossRef
13.
go back to reference McCourt M, Wang JH, Sookhai S, Redmond HP (2001) Activated human neutrophils release hepatocyte growth factor/scatter factor. Eur J Surg Oncol 27:396–403PubMedCrossRef McCourt M, Wang JH, Sookhai S, Redmond HP (2001) Activated human neutrophils release hepatocyte growth factor/scatter factor. Eur J Surg Oncol 27:396–403PubMedCrossRef
14.
go back to reference Jablonska E, Kiluk M, Markiewicz W, Piotrowski L, Grabowska Z, Jablonski J (2001) TNF-alpha, IL-6 and their soluble receptor serum levels and secretion by neutrophils in cancer patients. Arch Immunol Ther Exp (Warsz) 49:63–69 Jablonska E, Kiluk M, Markiewicz W, Piotrowski L, Grabowska Z, Jablonski J (2001) TNF-alpha, IL-6 and their soluble receptor serum levels and secretion by neutrophils in cancer patients. Arch Immunol Ther Exp (Warsz) 49:63–69
15.
go back to reference Schaider H, Oka M, Bogenrieder T et al (2003) Differential response of primary and metastatic melanomas to neutrophils attracted by IL-8. Int J Cancer 103:335–343PubMedCrossRef Schaider H, Oka M, Bogenrieder T et al (2003) Differential response of primary and metastatic melanomas to neutrophils attracted by IL-8. Int J Cancer 103:335–343PubMedCrossRef
16.
go back to reference Shamamian P, Schwartz JD, Pocock BJ et al (2001) Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis. J Cell Physiol 189:197–206PubMedCrossRef Shamamian P, Schwartz JD, Pocock BJ et al (2001) Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis. J Cell Physiol 189:197–206PubMedCrossRef
17.
go back to reference Scapini P, Nesi L, Morini M et al (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J Immunol 168:5798–5804PubMed Scapini P, Nesi L, Morini M et al (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J Immunol 168:5798–5804PubMed
18.
go back to reference Bambury RM, Teo MY, Power DG et al (2013) The association of pre-treatment neutrophil to lymphocyte ratio with overall survival in patients with glioblastoma multiforme. J Neurooncol 114:149–154PubMedCrossRef Bambury RM, Teo MY, Power DG et al (2013) The association of pre-treatment neutrophil to lymphocyte ratio with overall survival in patients with glioblastoma multiforme. J Neurooncol 114:149–154PubMedCrossRef
19.
go back to reference Polley MY, Lamborn KR, Chang SM et al (2010) Six-month progression-free survival as an alternative primary efficacy endpoint to overall survival in newly diagnosed glioblastoma patients receiving temozolomide. Neuro Oncol 12:274–282PubMedCentralPubMedCrossRef Polley MY, Lamborn KR, Chang SM et al (2010) Six-month progression-free survival as an alternative primary efficacy endpoint to overall survival in newly diagnosed glioblastoma patients receiving temozolomide. Neuro Oncol 12:274–282PubMedCentralPubMedCrossRef
20.
go back to reference Hosmer DW, Lemeshow S, May S (2008) Applied survival analysis: regression modeling of time to event data. Wiley, New YorkCrossRef Hosmer DW, Lemeshow S, May S (2008) Applied survival analysis: regression modeling of time to event data. Wiley, New YorkCrossRef
21.
go back to reference Gondo T, Nakashima J, Ohno Y et al (2012) Prognostic value of neutrophil-to-lymphocyte ratio and establishment of novel preoperative risk stratification model in bladder cancer patients treated with radical cystectomy. Urology 79:1085–1091PubMedCrossRef Gondo T, Nakashima J, Ohno Y et al (2012) Prognostic value of neutrophil-to-lymphocyte ratio and establishment of novel preoperative risk stratification model in bladder cancer patients treated with radical cystectomy. Urology 79:1085–1091PubMedCrossRef
22.
go back to reference Helseth R, Helseth E, Johannesen TB et al (2010) Overall survival, prognostic factors, and repeated surgery in a consecutive series of 516 patients with glioblastoma multiforme. Acta Neurol Scand 122:159–167PubMedCrossRef Helseth R, Helseth E, Johannesen TB et al (2010) Overall survival, prognostic factors, and repeated surgery in a consecutive series of 516 patients with glioblastoma multiforme. Acta Neurol Scand 122:159–167PubMedCrossRef
23.
go back to reference Terasaki M, Ogo E, Fukushima S et al (2007) Impact of combination therapy with repeat surgery and temozolomide for recurrent or progressive glioblastoma multiforme: a prospective trial. Surg Neurol 68:250–254PubMedCrossRef Terasaki M, Ogo E, Fukushima S et al (2007) Impact of combination therapy with repeat surgery and temozolomide for recurrent or progressive glioblastoma multiforme: a prospective trial. Surg Neurol 68:250–254PubMedCrossRef
24.
go back to reference Yovino S, Grossman SA (2012) Severity, etiology and possible consequences of treatment-related lymphopenia in patients with newly diagnosed high-grade gliomas. CNS Oncol 1:149–154PubMedCentralPubMedCrossRef Yovino S, Grossman SA (2012) Severity, etiology and possible consequences of treatment-related lymphopenia in patients with newly diagnosed high-grade gliomas. CNS Oncol 1:149–154PubMedCentralPubMedCrossRef
25.
go back to reference Cedres S, Torrejon D, Martinez A et al (2012) Neutrophil to lymphocyte ratio (NLR) as an indicator of poor prognosis in stage IV non-small cell lung cancer. Clin Transl Oncol 14:864–869PubMedCrossRef Cedres S, Torrejon D, Martinez A et al (2012) Neutrophil to lymphocyte ratio (NLR) as an indicator of poor prognosis in stage IV non-small cell lung cancer. Clin Transl Oncol 14:864–869PubMedCrossRef
26.
go back to reference Kao SC, Pavlakis N, Harvie R et al (2010) High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy. Clin Cancer Res 16:5805–5813PubMedCrossRef Kao SC, Pavlakis N, Harvie R et al (2010) High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy. Clin Cancer Res 16:5805–5813PubMedCrossRef
27.
go back to reference Brandes AA, Franceschi E, Tosoni A et al (2010) O6-Methylguanine DNA-methyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neuro Oncol 12:283–288PubMedCentralPubMedCrossRef Brandes AA, Franceschi E, Tosoni A et al (2010) O6-Methylguanine DNA-methyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neuro Oncol 12:283–288PubMedCentralPubMedCrossRef
28.
go back to reference Park JK, Hodges T, Arko L et al (2010) Scale to predict survival after surgery for recurrent glioblastoma multiforme. J Clin Oncol 28:3838–3843PubMedCrossRef Park JK, Hodges T, Arko L et al (2010) Scale to predict survival after surgery for recurrent glioblastoma multiforme. J Clin Oncol 28:3838–3843PubMedCrossRef
29.
go back to reference Grossman SA, Ye X, Lesser G et al (2011) Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res 17:5473–5480PubMedCentralPubMedCrossRef Grossman SA, Ye X, Lesser G et al (2011) Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res 17:5473–5480PubMedCentralPubMedCrossRef
30.
go back to reference Carro MS, Lim WK, Alvarez MJ et al (2010) The transcriptional network for mesenchymal transformation of brain tumours. Nature 463:318–325PubMedCrossRef Carro MS, Lim WK, Alvarez MJ et al (2010) The transcriptional network for mesenchymal transformation of brain tumours. Nature 463:318–325PubMedCrossRef
Metadata
Title
Factors impacting survival following second surgery in patients with glioblastoma in the temozolomide treatment era, incorporating neutrophil/lymphocyte ratio and time to first progression
Authors
Mairéad G. McNamara
Zarnie Lwin
Haiyan Jiang
Arnoud J. Templeton
Gelareh Zadeh
Mark Bernstein
Caroline Chung
Barbara-Ann Millar
Normand Laperriere
Warren P. Mason
Publication date
01-03-2014
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 1/2014
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-014-1366-9

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