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Diagnostic Value of Alpha-Fetoprotein Combined with Neutrophil-To Hu et al. BMC Gastroenterology (2018) 18:186 https://doi.org/10.1186/s12876-018-0908-6 RESEARCH ARTICLE Open Access Diagnostic value of alpha-fetoprotein combined with neutrophil-to-lymphocyte ratio for hepatocellular carcinoma Jian Hu1†, Nianyue Wang2†, Yongfeng Yang2,LiMa2, Ruilin Han3, Wei Zhang4, Cunling Yan3*, Yijie Zheng5* and Xiaoqin Wang1* Abstract Background: To investigate the diagnostic performance of alpha-fetoprotein (AFP) and neutrophil-to-lymphocyte ratio (NLR) as well as their combinations with other markers. Methods: Serum aspartate aminotransferase (AST), alanine aminotransferase (ALT), AFP and levels as well as the numbers of neutrophils and lymphocytes of all enrolled patients were collected. The NLR was calculated by dividing the number of neutrophils by the number of lymphocytes. Receiver operating characteristic (ROC) curve analysis was conducted to determine the ability of each marker and combination of markers to distinguish HCC and liver disease patients. Results: In total, 545 patients were included in this study. The area under the ROC curve (AUC) values for AFP, ALT, AST, and NLR were 0.775 (0.738–0.810), 0.504 (0.461–0.547), 0.660 (0.618–0.699), and 0.738 (0.699–0.774) with optimal cut-off values of 24.6 ng/mL, 111 IU/mL, 27 IU/mL, and 2.979, respectively. Of the four biomarkers, AFP and NLR showed comparable specificity (0.881 and 0.858) and sensitivity (0.561 and 0.539). The combination of AFP and NLR showed the highest AUC (0.769) with a significantly higher sensitivity (0.767) and a lower specificity (0.773) compared to AFP or NLR alone, and it had the highest sum of sensitivity and specificity (1.54) among all combinations. In patients with AFP < 20 ng/mL, the NLR showed the highest AUC and combination with other markers did not improve the diagnostic accuracy. Conclusions: Our data indicate that the combination of AFP and NLR offers better diagnostic performance than either marker alone for differentiating HCC from liver disease, which may benefit clinical screening. Keywords: Alpha-fetoprotein, Neutrophil-granulocyte ratio, Hepatocellular carcinoma Background stage and is associated with a poor prognosis, with a 5-year Liver cancer is the sixth most common cancer and the third overall survival rate of less than 15% [3, 4]. At present, leading cause of cancer-related death worldwide [1, 2]. He- treatments such as surgery and liver transplantation for patocellular carcinoma (HCC), which accounts for 70–85% early-stage HCC result in better outcomes with a 5-year of liver cancer cases, is always diagnosed in an advanced overall survival rate of more than 70% [5–7]. Therefore, diagnosis of HCC during an early stage is pivotal for im- * Correspondence: [email protected]; [email protected]; proving the clinical outcomes of patients. [email protected] † Alpha-fetoprotein (AFP) is the most widely used serum Jian Hu and Nianyue Wang contributed equally to this work. marker for screening and initial diagnosis of HCC in clin- 3Department of Clinical Laboratory, Peking University First Hospital, Beijing 100000, China ical practice. However, the sensitivity of AFP is only about 5Medical Scientific Affairs, Abbott Diagnostics Division, Abbott Laboratories, 60% at a cut-off value of 20 ng/mL, and the specificity is Shanghai 200032, China low [8–10]. Moreover, AFP levels remain normal in 15– 1Department of Clinical Laboratory, The First Affiliated Hospital of Xi’an Jiaotong University, 277 West Yanta Road, Xi’an 710061, People’s Republic of 30% of patients with advanced stage disease and increase China in some patients with chronic hepatitis, liver cirrhosis, and Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Hu et al. BMC Gastroenterology (2018) 18:186 Page 2 of 7 other liver diseases [4, 11], leading to high negative and and treatment-naïve patients with HCC were enrolled in false-positive rates. Therefore, novel markers that comple- the present study. Liver disease samples were mainly ment the limitations of AFP are needed to for screening from patients infected with hepatitis B virus (HBV) or and more accurate diagnosis of HCC. hepatitis C virus (HCV) and include samples from pa- Crosstalk between cancer cells and their inflammatory tients with hepatitis and cirrhosis, which were diagnosed microenvironment plays critical roles in the initiation and according to APASL guideline. progression of cancer, including the promotion of angio- This study was conducted according to the Declaration genesis, proliferation, and metastasis [12–14]. Inflammatory of Helsinki and approved by the Ethics of Committee. infiltrates in the tumor microenvironment largely influence the biological behavior of HCC [15–18]. The Data collection neutrophil-to-lymphocyte ratio (NLR) is one parameter Serum AST and ALT concentrations and the numbers of reflecting the presence of a systemic inflammatory response neutrophils and lymphocytes were recorded from routine and can be readily determined at low cost through routine clinical testing. Serum AFP was measured using the Abbott blood examination. The baseline NLR has been reported to ARCHITECT hepatitis B surface antigen chemiluminescent be a valuable predictor in many cancers, including colorectal microparticle immunoassay (Abbott Diagnostics, Abbott cancer [19], renal cancer [20], diffuse large B-cell lymphoma Park, IL, USA). The NLR was calculated by dividing the [21, 22], and HCC [23]. The NLR also has been reported to number of neutrophils by the number of lymphocytes. be diagnostic marker for peptic ulcer perforation [24], acute mesenteric ischemia [25], and lung cancer [26, 27]. Statistical analysis Thus, we questioned whether the NLR can be used as All statistical analyses were performed using SPSS (version a supplementary diagnostic marker with AFP. This study 21; IBM, Armonk, NY, USA). Data are presented as mean aimed to evaluate the diagnostic value of AFP in com- ± standard derivation for normally distributed continuous bination with the NLR for HCC. To better investigate data, as median (interquartile range, Q25–Q75) for abnor- the relative diagnostic value of serum biomarkers, two mally distributed continuous data, or as actual values for common serum biomarkers for liver function, aspartate categorical data. Comparisons between two groups were aminotransferase (AST) and alanine aminotransferase performed using t test, Wilcoxon test, or chi-square test. (ALT), also were analyzed in the present study. Receiver operation characteristic (ROC) curves were used to compare the diagnostic performance of each biomarker. Methods The area under the ROC curve (AUC) for each biomarker Patients for distinguishing HCC and liver disease patients as well Patients diagnosed with HCC and liver disease were as the optimal cut-off value, sensitivity, specificity, positive enrolled at the three centers (Peking University 1st Hos- predictive value (PPV), and negative predictive value pital, Xi’an Jiaotong University 1st Hospital and The Sec- (NPV) were calculated using MedCalc. Combinations of ond Hospital of Nanjing, Affiliated to Medical School of markers were analyzed, and the related parameters were cal- Southeast University) between July 2013 and July 2016. culated with the online statistical software OpenEpi (http:// HCC was diagnosed according to the Asian Pacific Asso- www.openepi.com/Menu/OE_Menu.htm). A P value < 0.05 ciation for the Study of the Liver (APASL) consensus was considered to indicate a statistically significant recommendations on HCC [28]. Only newly diagnosed difference. Table 1 Clinical characteristics of the patients Liver disease (n = 176) HCC (n = 369) P value Age (y) 46.34 ± 11.71 56.91 ± 10.04 < 0.001 Gender (M/F) 124/52 318/51 < 0.001 Neutrophils (× 109/L) 5.705 (2.97–58.20) 0.674 (0.57–0.78) < 0.001 Lymphocytes (× 109/L) 3.01 (1.65–30.85) 0.209 (0.12–0.295) < 0.001 NLR 1.851 (1.43–2.53) 3.23 (1.91–6.62) < 0.001 ALT (IU/mL) 38.5 (26.00–66.50) 38.9 (23.75–73.93) 0.739 AST (IU/mL) 29 (21.00–52.00) 44 (29.78–85.65) < 0.001 AFP (ng/mL) 3.67 (2.43–10.36) 41.16 (5.59–1030.03) < 0.001 HCC, hepatocellular carcinoma; M, male; F, female; NLR, neutrophil-granulocyte ratio; ALT, alanine aminotransferase; AST, aspartate aminotransferase; AFP, alpha-fetoprotein Data are presented as mean ± standard derivation for age, actual values for gender, and median (interquartile range, Q25-Q75) for other parameters Comparisons between two groups were performed using t test for age, chi-square test for gender, or Wilcoxon test for other parameters Hu et al. BMC Gastroenterology (2018) 18:186 Page 3 of 7 Diagnostic accuracy of serum biomarkers for detecting HCC The ROC curves for serum biomarkers (AFP, ALT, AST, and NLR) for diagnosing HCC are shown in Fig. 1. The AUC values for AFP, ALT, AST, and NLR were 0.775 (0.738–0.810), 0.504 (0.461–0.547), 0.660 (0.618–0.699), and 0.738 (0.699–0.774) with optimal cut-off values of 24.6 ng/mL, 111 IU/mL, 27 IU/mL, and 2.979, respect- ively. When applying the common cutoff value of 20 ng/ mL for AFP, the AUC was 0.664 (0.6224–0.703) (Table 2). Of the four biomarkers, ALT showed the highest specifi- city (0.909) with the lowest sensitivity (0.184), and AFP and NLR individually showed both higher specificity (0.881 and 0.858) and higher sensitivity (0.561 and 0.539) compared to AST (Table 2).
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