18F-FDG texture analysis predicts the pathological Fuhrman nuclear grade of clear cell renal cell carcinoma

Abdominal Radiology https://doi.org/10.1007/s00261-021-03246-x KIDNEYS, URETERS, BLADDER, RETROPERITONEUM 18 F‑FDG texture analysis predicts the pathological Fuhrman nuclear grade of clear cell renal cell carcinoma Linhan Zhang1 · Hongyue Zhao1 · Huijie Jiang2 · Hong Zhao3 · Wei Han1 · Mengjiao Wang1 · Peng Fu1 Received: 17 March 2021 / Revised: 8 August 2021 / Accepted: 9 August 2021 © The Author(s) 2021 Abstract Purpose This article analyzes the image heterogeneity of clear cell renal cell carcinoma (ccRCC) based on positron emission tomography (PET) and positron emission tomography-computed tomography (PET/CT) texture parameters, and provides a new objective quantitative parameter for predicting pathological Fuhrman nuclear grading before surgery. Methods A retrospective analysis was performed on preoperative PET/CT images of 49 patients whose surgical pathology was ccRCC, 27 of whom were low grade (Fuhrman I/II) and 22 of whom were high grade (Fuhrman III/IV). Radiological parameters and standard uptake value (SUV) indicators on PET and computed tomography (CT) images were extracted by using the LIFEx software package. The discriminative ability of each texture parameter was evaluated through receiver operating curve (ROC). Binary logistic regression analysis was used to screen the texture parameters with distinguishing and diagnostic capabilities and whose area under curve (AUC) > 0.5. DeLong's test was used to compare the AUCs of PET texture parameter model and PET/CT texture parameter model with traditional maximum standardized uptake value (SUVmax) model and the ratio of tumor SUVmax to liver SUVmean (SUL)model. In addition, the models with the larger AUCs among the SUV models and texture models were prospectively internally verified. Results In the ROC curve analysis, the AUCs of SUVmax model, SUL model, PET texture parameter model, and PET/CT texture parameter model were 0.803, 0.819, 0.873, and 0.926, respectively. The prediction ability of PET texture parameter model or PET/CT texture parameter model was significantly better than SUVmax model (P = 0.017, P = 0.02), but it was not better than SUL model (P = 0.269, P = 0.053). In the prospective validation cohort, both the SUL model and the PET/ CT texture parameter model had good predictive ability, and the AUCs of them were 0.727 and 0.792, respectively. Conclusion PET and PET/CT texture parameter models can improve the prediction ability of ccRCC Fuhrman nuclear grade; SUL model may be the more accurate and easiest way to predict ccRCC Fuhrman nuclear grade. * Huijie Jiang * Peng Fu 1 Department of Nuclear Medicine, The First Affiliated Hospital of Harbin Medical University, Harbin, China 2 Department of Radiology, The Second Affiliated Hospital of Harbin Medical University, Harbin, China 3 Department of Nuclear Medicine, ShenZhen People’s Hospital, ShenZhen, China 13 Vol.:(0123456789) Abdominal Radiology Graphic abstract Keywords Adenocarcinoma · Clear cell · Fuhrman grade · Fluorodeoxyglucose F18 · Radiomics Introduction According to the cases announced by the American Cancer Society in 2021, the number of new kidney cancer cases was 76,080, and the number of new kidney cancer deaths was 13,780 [1]. Renal cell carcinoma accounts for about 80% of all kidney cancers. Saad et al. [2] conducted an epidemiological study of renal cell carcinoma in the USA in the past 20 years. They found that the incidence of renal cell carcinoma remained stable since 2008 and the overall mortality rate began to decline since 2001. However, as the most common subtype of renal cell carcinoma, clear cell renal cell carcinoma (ccRCC) had a continuously increasing incidence and its mortality rate did not decline until 2012. Therefore, research on ccRCC is of great significance to improve the cure rate of renal tumors. Fuhrman nuclear grade is a recognized prognostic indicator of ccRCC. Studies have shown that [3, 4] low grade ccRCC is associated with a good prognosis and high grade ccRCC is associated with higher infiltration capacity, higher possibility of metastasis, and poor prognosis. In addition, there is a significant difference in the recurrence rate of ccRCC between high grade and low grade patients after surgery, and the risk of recurrence after surgery for higher grade tumors is significantly increased [5]. Therefore, the prediction of ccRCC grade is helpful for clinicians to plan management decisions. In the simplified 13 Fuhrman nuclear grading system, ccRCC cases are divided into low grade (Fuhrman I/II) and high grade (Fuhrman III/ IV), which not only reduces the difference between observers, improves repeatability, saves time and money, but also does not affect the ability to predict cancer-specific mortality [6]. Imaging-guided fine-needle aspiration biopsy is the gold standard for preoperative renal tumor grading. However, due to the high spatiotemporal heterogeneity of ccRCC, the biopsy tissue only represents a part of the lesion, which may lead to selection bias and cannot well reflect the Fuhrman nuclear grade of the entire tumor. Moreover, this invasive operation has disadvantages such as poor repeatability and complications. Therefore, non-invasive methods are essential for the preoperative evaluation of ccRCC. Due to the Warburg effect of malignant tumors, the glucose transporter 1 (GLUT1) is up-regulated, and other enzymes are over-expressed, especially lactate dehydrogenase (LDH), which appear as hypermetabolic foci on 18 F-fluorodeoxyglucose ( 18F-FDG) positron emission tomography—computed tomography (PET/CT). Therefore, PET/CT is widely used in the diagnosis, grading, monitoring of treatment response, efficacy evaluation, and prognosis determination of various tumors. However, ccRCC does not have the typical Warburg effect, and 18F-FDG is excreted through the kidneys. It is difficult to distinguish between tumor metabolism and background. Therefore, in the professional practice guidelines issued by American Urological Abdominal Radiology Association (AUA), and European Society for Medical Oncology (ESMO) and European Association of Urology (EAU), it is generally not recommended to use FDG as a kidney tumor imaging agent [7–9]. But this does not mean that PET/CT examination is useless for the diagnosis of ccRCC. A number of studies have shown that the value of maximum standardized uptake value (SUVmax) as the traditional PET/ CT parameter has a certain correlation with the Fuhrman grade of pathology [10–12]. Radiomics that have emerged in recent years can establish models by using a large amount of high-throughput information obtained by image segmentation and feature extraction of regions of interest (ROI) in computed tomography (CT), magnetic resonance imaging (MRI), positron emission tomography (PET), and other images. The researchers input the patient's medical images into computer software with mathematical algorithm functions, and obtain quantitative radiomics characteri (...truncated)