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Clinical Evaluation of 99Mtc-Rituximab for Sentinel Lymph Node Mapping in Breast Cancer Patients

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Clinical Evaluation of 99Mtc-Rituximab for Sentinel Lymph Node Mapping in Breast Cancer Patients Journal of Nuclear Medicine, published on March 16, 2016 as doi:10.2967/jnumed.115.160572 Clinical Evaluation of 99mTc-Rituximab for Sentinel Lymph Node Mapping in Breast Cancer Patients Nan Li1,#, Xuejuan Wang1,#, Baohe Lin1, Hua Zhu1, Cheng Liu1, Xiaobao Xu1, Yan Zhang1, Shizhen Zhai1, Tao OuYang2, Jinfeng Li2, Zhi Yang1 Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), 1Department of Nuclear Medicine, 2Breast Center, Peking University Cancer Hospital & Institute, Beijing 100142, China Running title: 99mTc-Rituximab for SLN Mapping Nan Li# , E-mail: [email protected] Xuejuan Wang#, E-mail: [email protected] # These two authors contributed to this study equally For correspondence to: Nan Li, Department of Nuclear Medicine, Beijing Cancer Hospital, No 52 Fucheng Rd, Beijing, 100142, China. E-mail: [email protected] Zhi Yang, Department of Nuclear Medicine, Beijing Cancer Hospital, No 52 Fucheng Rd, Beijing, 100142, China. Email: [email protected] Word counts: 4887 1 ABSTRACT The metastatic status of sentinel lymph nodes (SLN) might be the most important prognostic factor in breast cancer. In this paper, we report the first study of 99mTc-Rituximab as a radiotracer for imaging of SLN using lymphoscintigraphy in both preoperative and intra-operative breast cancer patients. Method: 99mTc-Rituximab was designed as a novel SLN tracer targeting the CD20 antigen which expresses extensively in lymph nodes. A retrospective study was performed on 2317 patients with primary breast cancer who underwent the lymphoscintigraphy and SLNB (sentinel lymph node biopsy). Before imaging, all patients had preoperative peritumoral injection of 37 MBq of 99mTc-rituximab. Results: 99mTc-rituximab was synthesized in both high radiolabeling yield and high radiochemical purity (> 95%), with molecular integrity and immune activity well maintained. The initial study of 100 breast cancer patients showed that the success rate of SLN lymphoscintigraphy by injection of 99mTc-rituximab, as compared with SLNB, was 100%, and the sensitivity, specificity, accuracy and false negative rate, was 97.4%, 100% , 98.0%, and 2.60%, respectively. Of the following 2217 patients studied, the success rate of lymphoscintigraphy and SLNB was 98.8% and 99.9%, and the average number of SLN was 1.78 (ranging from 1 to 10) and 2.85 (ranging from 1 to 15). Age is independent predictor of the number of SLNs identified by lymphoscintigraphy and intraoperative handled gamma probe (p<0.05), and other factors, such as gender, imaging time, primary tumor site, histopathological subtype, clinical T stage, and immunochemistry, are not (p>0.05). However, the SLN metastatic rates were different in patients with different histopathological subtype, clinical T stage, and immunochemistry (p<0.05). Conclusion: Here we report the first study of the new radiotracer 99mTc-Rituximab for breast cancer lymphoscintigraphy. This new tracer showed great feasibility, safety and effectiveness for SLN mapping in breast cancer patients. Keywords: 99mTc-Rituximab, sentinel lymph node mapping, breast cancer, lymphoscintigraphy 2 INTRODUCTION Accurate lymph node staging is essential for the prognosis and treatment of cancer patients. SLN is defined as the first node or nodes in the lymphatic drainage of the primary tumor, which was created by Gould et al in 1960 (1). In 1977, Cabanas suggested that the SLN would be predictive of metastatic spread to the respective regional lymphatic basins (2). SLN mapping also enables surgeons to perform a minimal invasive biopsy of the SLN and to complete resect all SLNs, and in the past two decades, the detection and biopsy of SLN have already been implemented in the surgical treatment of breast cancer and malignant melanoma patients (3,4). Visual examination with blue dyes and lymphoscintigraphy has been extensively used for SLN mapping in clinic (5). Isosulfan blue and methylene blue are two commonly used blue dyes in the SLN biopsy of breast cancer. Actually, methylene blue is the most commonly used SLN mapping agent in China. However, the small molecule blue dyes migrate very rapidly in the lymphatics, and the retention of dye in SLNs is poor (less than 5 min) (6). So, it’s essential for surgeon to locate and remove the SLNs quickly before the dye spreads to other nodes. Moreover, the blue dyes may also cause unwanted anaphylactic side effects, and make blue discoloration of urine, stool and skin in some patients (7). For lymphoscintigraphy, a variety of radiopharmaceuticals have been used including the filtered and unfiltered 99mTc sulfur colloid, 99mTc labeled albumin-based colloids, 99mTc antimony trisulfide colloid. For all these colloid based imaging techniques, SLN visualization depends on the transport of the radiolabeled particles from the injection site to SLN through lymphatic channels (8). The radiolabeled particles are then trapped in the node and absorbed by macrophages. The detection rate for these 99mTc-radiopharmaceuticals ranges from 86% to 99% (9,10), which is mainly caused by that many factors, such as particle size, particle concentration, and injection dose can influence the transport and accumulation process of the tracer (11-13). In 2013, The U.S. Food and Drug Administration approved Lymphoseek® (99mTc-tilmanocept) as the radiotracer for detecting SLN in breast cancer and melanoma patients (14,15). The success of Lymphoseek encourages us to report other receptor targeted SLN imaging 3 agent. Rituximab is a chimeric monoclonal antibody against the CD20 antigen presenting on the membrane of pre-B and mature B lymphocytes. It was approved by the Food and Drug Administration in 1997 to treat B-cell non-Hodgkin lymphomas resistant to chemotherapy regimens (16,17). Considering there are large number of B cells presenting in lymph nodes, we hypothesized that radiolabeled Rituximab can serve as an effective imaging tool for SLN identification. Therefore in this work, Rituximab was directly labeled the mostly widely used single photon emission computed tomography (SPECT) radionuclide 99mTc. The resulted tracer, 99mTc-Rituxmab, was further evaluated in a large cohort of breast cancer patients (total number of patients = 2317). Here the feasibility, effectiveness and safety of using 99mTc-Rituxmab for clinical imaging of SLN were reported. MATERIALS and METHODS Patients The criterion for inclusion and exclusion of patients meets standard SLN biopsy criteria (supplemental material). The clinic trial was approved by Peking University Cancer Hospital & Institute. From July 2005 to June 2011, patients with breast cancer were recruited at Peking University Cancer Hospital & Institute. The patients’ informed consents were obtained before the tests. SLN imaging was performed totally in 2317 breast cancer patients using 99mTc-Rituximab followed by SLN biopsy to verify the imaging results. Radiotracer Preparation 99mTc radiolabeling of Rituximab and radio highperformance liquid chromatography (HPLC) analysis was performed as described (Supplemental Figs. 1-3). Briefly, Rituximab (10 mg, 70 nmol) was dissolved in 1 mL of phosphate buffer solution (PBS) (pH =7.4, 10 mM), and 0.3 mL of the solution was taken out to react with 25 μL of 10% (V/V) 2-mercaptoethanol for 15 min in dark. The product was then purified by a PD10 column to obtain 2 mL reduced Rituximab, and 4 the solution was divided into 0.2 mL each vial, and the samples were stored at -20 oC for further use. When radiolabeling was performed, 0.2 mL solution of reduced Rituximab was warmed to room temperature and was added 10 μL of 100 mg/mL glucoheptonic acid, 15 μL of 1 mg/mL 99m SnCl2 and 370-470 MBq Na TcO4. The reaction mixture was shaken at room temperature for 10 min. 99mTc-Rituximab was then purified by a PD-10 column. For clinical use, the radiochemical purity of the tracer was always greater than 99% tested by radio- thin layer chromatography (TLC) and radio-HPLC. The radiotracer solution was then diluted to approximately 74 MBq/mL (2 mCi/mL) with saline and was filtered with a 0.20-µm Millex-LG filter (EMD Millipore). The synthesis of Rit-SH and radiolabeling with 99mTc were performed under good-manufacturing practice conditions with daily quality control. Each patient was injected with 37 MBq (1.0 mCi) of 99mTc-Rituximab. Lymphatic Mapping Protocol Guided by ultrasound, all patients had peritumoral subcutaneous injections of 99mTc-rituximab (37.0 MBq, 0.5mL) 2 to 18 hours before biopsy. In lymphoscintigraphy, three point sources (0.37 MBq) were put on the surface of the patient to mark the sternal notch, contralateral sternal margin, metasternum location as references. Planar lymphoscintigraphy was then acquired by a SPECT (Siemens, E.Cam, Germany) with the patient positioned supine in the anterior view and the ipsilateral lateral view, to determine the location and number of SLNs (Supplemental Figs. 4-8). Acquisition parameters as follows: low energy high resolution parallel hole collimator, energy peak 140 Kev, 20% window width, 128×128 matrix, zoom=1. Surgical Procedure After axillary incision, SLNs were identified by a handled gamma detecting probe (Crystal, USA). All radioactive nodes with a counting rate ≥10% of the hottest node were removed. During surgery, all the SLNs were evaluated by frozen-section analysis. During the initial learning period (100 patients), all the patients underwent an axillary lymph node dissection 5 (ALND). After initial learning, only patients with positive frozen sections immediately underwent an ALND. In order to evaluate the effectiveness and reliability of 99mTc-rituximab, another 2217 patients were divided into different groups to find the predictors of the number of SLNs identified. All the dissected SLNs and non-SLNs were analyzed by hematoxylin and eosin staining. Statistical Analysis All values were expressed as mean ± standard deviation. Statistical analysis was performed using the one-way analysis of variance or the chi-squared test by SPSS17.0. The differences between groups were considered to be significant when the p value were <0.05. RESULTS Synthesis of 99mTc-Rituximab 99m The radiolabeling yield is >95% using the freeze-dried kit of Rituximab and Na TcO4.
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