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Diagnostic Value of Preoperative Inflammatory Markers in Patients with Glioma: a Multicenter Cohort Study

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Diagnostic Value of Preoperative Inflammatory Markers in Patients with Glioma: a Multicenter Cohort Study CLINICAL ARTICLE J Neurosurg 129:583–592, 2018 Diagnostic value of preoperative inflammatory markers in patients with glioma: a multicenter cohort study *Shi-hao Zheng, MD,1 Jin-lan Huang, PhD,2,4 Ming Chen, MD,3 Bing-long Wang, BS,2 Qi-shui Ou, PhD,2 and Sheng-yue Huang, BS1 1Department of Neurosurgery, Fujian Provincial Hospital; 2Department of Clinical Laboratory, First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian; 3Department of Neurosurgery, Xin Hua Hospital, Affiliated with Shanghai Jiao Tong University School of Medicine, Shanghai; and 4Laboratory Medicine Center, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, People’s Republic of China OBJECTIVE Glioma is the most common form of brain tumor and has high lethality. The authors of this study aimed to elucidate the efficiency of preoperative inflammatory markers, including neutrophil/lymphocyte ratio (NLR), derived NLR (dNLR), platelet/lymphocyte ratio (PLR), lymphocyte/monocyte ratio (LMR), and prognostic nutritional index (PNI), and their paired combinations as tools for the preoperative diagnosis of glioma, with particular interest in its most aggressive form, glioblastoma (GBM). METHODS The medical records of patients newly diagnosed with glioma, acoustic neuroma, meningioma, or nonle- sional epilepsy at 3 hospitals between January 2011 and February 2016 were collected and retrospectively analyzed. The values of NLR, dNLR, PLR, LMR, and PNI were compared among patients suffering from glioma, acoustic neuroma, meningioma, and nonlesional epilepsy and healthy controls by using nonparametric tests. Correlations between NLR, dNLR, PLR, LMR, PNI, and tumor grade were analyzed. Receiver operating characteristic (ROC) curve analysis was performed to evaluate the diagnostic significance of NLR, dNLR, PLR, LMR, PNI, and their paired combinations for glioma, particularly GBM. RESULTS A total of 750 patients with glioma (Grade I, 81 patients; Grade II, 208 patients; Grade III, 169 patients; Grade IV [GBM], 292 patients), 44 with acoustic neuroma, 271 with meningioma, 102 with nonlesional epilepsy, and 682 healthy controls were included in this study. Compared with healthy controls and patients with acoustic neuroma, meningioma, or nonlesional epilepsy, the patients with glioma had higher values of preoperative NLR and dNLR as well as lower val- ues of LMR and PNI, whereas PLR was higher in glioma patients than in healthy controls and patients with nonlesional epilepsy. Subgroup analysis revealed a positive correlation between NLR, dNLR, PLR, and tumor grade but a negative correlation between LMR, PNI, and tumor grade in glioma. For glioma diagnosis, the area under the curve (AUC) ob- tained from the ROC curve was 0.722 (0.697–0.747) for NLR, 0.696 (0.670–0.722) for dNLR, 0.576 (0.549–0.604) for PLR, 0.760 (0.738–0.783) for LMR, and 0.672 (0.646–0.698) for PNI. The best diagnostic performance was obtained with the combination of NLR+LMR and dNLR+LMR, with AUCs of 0.777 and 0.778, respectively. Additionally, NLR (AUC 0.860, 95% CI 0.832–0.887), dNLR (0.840, 0.810–0.869), PLR (0.678, 0.641–0.715), LMR (0.837, 0.811–0.863), and PNI (0.740, 0.706–0.773) had significant predictive value for GBM compared with healthy controls and other disease groups. As compared with the Grade I–III glioma patients, the GBM patients had an AUC of 0.811 (95% CI 0.778–0.844) for NLR, 0.797 (0.763–0.832) for dNLR, 0.662 (0.622–0.702) for PLR, 0.743 (0.707–0.779) for LMR, and 0.661(0.622–0.701) for PNI. For the paired combinations, NLR+LMR demonstrated the highest accuracy. CONCLUSIONS The NLR+LMR combination was revealed as a noninvasive biomarker with relatively high sensitivity and specificity for glioma diagnosis, the differential diagnosis of glioma from acoustic neuroma and meningioma, GBM diagnosis, and the differential diagnosis of GBM from low-grade glioma. https://thejns.org/doi/abs/10.3171/2017.3.JNS161648 KEY WORDS glioma; glioblastoma; biomarkers; neutrophil lymphocyte ratio; lymphocyte monocyte ratio; oncology ABBREVIATIONS AUC = area under the curve; dNLR = derived NLR; GBM = glioblastoma; IL-10 = interleukin 10; LMR = lymphocyte/monocyte ratio; NLR = neutrophil/ lymphocyte ratio; PLR = platelet/lymphocyte ratio; PNI = prognostic nutritional index; ROC = receiver operating characteristic; TGF-b = tumor growth factor–b; WBC = white blood cell. SUBMITTED June 27, 2016. ACCEPTED March 17, 2017. INCLUDE WHEN CITING Published online November 3, 2017; DOI: 10.3171/2017.3.JNS161648. * Drs. Zheng, J. I. Huang, and Chen contributed equally to this work. ©AANS 2018, except where prohibited by US copyright law J Neurosurg Volume 129 • September 2018 583 Unauthenticated | Downloaded 10/09/21 11:14 PM UTC S. H. Zheng et al. LIOMA is the most frequent primary brain tumor, glioma, acoustic neuroma, meningioma, or nonlesional accounting for 81% of malignant brain and cen- epilepsy at 3 hospitals (Fujian Provincial Hospital, Guang- tral nervous system tumors.22 The most aggressive zhou Nangfang Hospital, Shanghai Xin Hua Hospital) Gand common type of glioma is glioblastoma (GBM; WHO between January 2011 and February 2016 were collect- Grade IV), with an annual incidence of approximately 3.5 ed and retrospectively analyzed. All patients included in cases in 100,000 people per year.13 Despite the therapeutic the analysis had to meet the following criteria: 1) glioma advances made in the past few decades, such as resection, and tumor grading histologically verified in a resection irradiation with adjuvant temozolomide, and experimental or biopsy specimen according to WHO criteria, acoustic chemotherapy, the overall 5-year survival rate of glioma neuroma and meningioma histologically proven in a re- patients remains poor.22,28 In particular, GBM patients section, or nonlesional epilepsy verified according to the have the poorest overall survival, with a median survival practical clinical definition of epilepsy developed by the 1 of only 12–15 months. Currently, histological examina- International League Against Epilepsy (ILAE) in 2014; tion of tumor tissue obtained at biopsy or resection serves 2) no prior cancer-specific pretreatment, such as chemo- as the standard procedure for definitive diagnosis of gli- therapy or radiotherapy; 3) no hematological disease, cur- oma, whereas CT and MRI are supplemental procedures 1,21 rent infectious disease, hyperpyrexia, diabetes mellitus, for disease staging and treatment response monitoring. metabolic syndrome, serious heart disease, hypertension, However, both the histopathological and neuroimaging severe renal or hepatic dysfunction, other cancer, autoim- tests are insensitive and expensive and can cause hemor- 23 mune disease, inflammatory disease, or medication usage rhage or neurological damage. Moreover, unlike other related to an inflammatory condition; 4) complete data on cancers such as prostate cancer, glioma has no sensitive or preoperative blood count and serum albumin levels; and specific serum marker that has been clinically applied for 5) informed consent. Ultimately, 750 patients with glioma, its detection, disease staging, treatment response monitor- 44 with acoustic neuroma, 271 with meningioma, and 102 ing, and prognosis.17,29 Thus, there is an urgent need for with nonlesional epilepsy were included in the analysis. minimally invasive biomarkers with improved sensitiv- ity and specificity and lower costs for glioma, especially For the control group, we reviewed the records of 682 age- GBM. and sex-matched healthy individuals who had undergone Emerging studies have highlighted the crucial role of their annual health check at the hospital. This study was the host inflammatory response in cancer progression approved by the institutional ethics committee. and prognosis.19 Generally, the inflammatory response is characterized by changes in the levels of white blood cells Data Collection (WBCs), neutrophils, lymphocytes, monocytes, platelets, Demographic and clinicopathological variables, includ- C-reactive protein, and albumin.5,6 These blood parameters ing age, sex, tumor grade, histological type, and so forth, are simple, low cost, and easy to measure with widely used were retrieved from the patient medical records. Within 1 and standardized assays. Various combinations of these week of surgery, blood samples were routinely taken for a factors have been measured to derive inflammation-based blood test and hepatic function test as part of the standard scores, including neutrophil/lymphocyte ratio (NLR), de- preoperative workup. All tests were performed by staff in rived NLR (dNLR), platelet/lymphocyte ratio (PLR), lym- the clinical laboratory department within 2 hours of col- phocyte/monocyte ratio (LMR), and prognostic nutritional lection. The WBC, neutrophil, lymphocyte, monocyte, and index (PNI). Recently, all 5 of these markers have been platelet counts were collected from the routine blood test, proven to refine stratification of patients to treatment and and albumin levels were collected from the hepatic func- predict survival in various cancers.5,9,24 As regards glioma, tion test. Moreover, preoperative NLR (quotient of neutro- an increase in preoperative NLR has been linked to poorer phil count to lymphocyte count), dNLR (quotient of [WBC survival in GBM patients enrolled in 2 cohort studies.3,12 count – neutrophil count] to lymphocyte count), PLR (ra- Moreover, McNamara et al. have reported that an NLR > tio of platelet count to lymphocyte count), LMR (ratio of 4 prior to a second surgery is a poor
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