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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 Clinical Evaluation of 99mTc-Rituximab for Sentinel Lymph Node Mapping in Breast Cancer Patients Nan Li*1, Xuejuan Wang*1, Baohe Lin1, Hua Zhu1, Cheng Liu1, Xiaobao Xu1, Yan Zhang1, Shizhen Zhai1, Tao OuYang2, Jinfeng Li2, and Zhi Yang1 1Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Nuclear Medicine, Peking University Cancer Hospital & Institute, Beijing, China; and 2Breast Center, Peking University Cancer Hospital & Institute, Beijing, China The metastatic status of sentinel lymph nodes (SLNs) might be the Accurate lymph node (LN) staging is essential for the prog- most important prognostic factor in breast cancer. In this paper, we nosis and treatment of cancer patients. The term sentinel lymph 99m report to our knowledge the first study of Tc-rituximab as a node (SLN) is defined as the first node or nodes in the lymphatic radiotracer for imaging of SLNs using lymphoscintigraphy in both pre- drainage of the primary tumor and was so named by Gould et al. operative and intraoperative breast cancer patients. Methods: 99mTc- rituximab was designed as an SLN tracer targeting the CD20 antigen, in 1960 (1). In 1977, Cabanas suggested that the SLN would be which expresses extensively in LNs. A retrospective study was per- predictive of metastatic spread to the respective regional lym- formed on 2,317 patients with primary breast cancer who underwent phatic basins (2). SLN mapping also enables surgeons to perform lymphoscintigraphy and sentinel lymph node biopsy (SLNB). Before a minimally invasive biopsy of the SLN and to completely resect imaging, all patients were administered a preoperative peritumoral in- all SLNs, and in the past 2 decades, the detection and biopsy of jection of 37 MBq of 99mTc-rituximab. Results: 99mTc-rituximab was SLNs have already been implemented in the surgical treatment of synthesized in both high radiolabeling yield and high radiochemical breast cancer and malignant melanoma patients (3,4). purity ( 95%), with molecular integrity and immune activity well main- Visual examination with blue dyes and lymphoscintigraphy has tained. The initial study of 100 breast cancer patients showed that the been extensively used for SLN mapping in the clinic (5). Isosulfan success rate of SLN lymphoscintigraphy by injection of 99mTc-rituximab, as compared with SLNB, was 100%, and the sensitivity, specificity, blue and methylene blue are 2 commonly used blue dyes in the accuracy, and false negative rate were 97.4%, 100%, 98.0%, and SLN biopsy of breast cancer. Actually, methylene blue is the most 2.60%, respectively. Of the following 2,217 patients studied, the suc- commonly used SLN mapping agent in China. However, the cess rate of lymphoscintigraphy and SLNB was 98.8% and 99.9%, small-molecule blue dyes migrate rapidly in the lymphatics, and and the average number of SLN was 1.78 (range, 1–10) and 2.85 the retention of dye in SLNs is poor (,5 min) (6). So, it is – (range, 1 15). Age was an independent predictor of the number of essential for surgeons to locate and remove the SLNs quickly SLNs identified by lymphoscintigraphy and intraoperative handheld before the dye spreads to other nodes. Moreover, the blue dyes γ-probe (P , 0.05), and other factors—such as sex, imaging time, primary tumor site, histopathologic subtype, clinical T stage, and may also cause unwanted anaphylactic side effects and cause blue immunochemistry—were not (P . 0.05). However, the SLN metastatic discoloration of urine, stool, and skin in some patients (7). For rates were different in patients with different histopathologic subtype, lymphoscintigraphy, a variety of radiopharmaceuticals has been clinical T stage, and immunochemistry (P , 0.05). Conclusion: Here used including the filtered and unfiltered 99mTc-sulfur colloid, we report the first study of the new radiotracer 99mTc-rituximab for 99mTc-labeled albumin-based colloids, and 99mTc-antimony trisul- breast cancer lymphoscintigraphy. This tracer showed great feasibility, fide colloid. For all these colloid-based imaging techniques, SLN safety, and effectiveness for SLN mapping in breast cancer patients. visualization depends on the transport of the radiolabeled particles Key Words: 99mTc-rituximab; sentinel lymph node mapping; breast from the injection site to SLNs through lymphatic channels (8). cancer; lymphoscintigraphy The radiolabeled particles are then trapped in the node and J Nucl Med 2016; 57:1214–1220 absorbed by macrophages. The detection rate of these 99mTc DOI: 10.2967/jnumed.115.160572 radiopharmaceuticals (range, 86%–99%) (9,10) is mainly caused by many factors, such as particle size, particle concentration, and injection dose, that can influence the transport and accumulation process of the tracer (11–13). In 2013, The U.S. Food and Drug Administration approved 99m Received May 14, 2015; revision accepted Feb. 18, 2016. Lymphoseek ( Tc-tilmanocept; Navidea Biopharmaceuticals, For correspondence or reprints contact either of the following: Inc.) as the radiotracer for detecting SLN in breast cancer and Nan Li, Department of Nuclear Medicine, Beijing Cancer Hospital, No. 52 Fucheng Rd., Beijing, 100142, China. melanoma patients (14,15). The success of Lymphoseek encour- E-mail: [email protected] ages us to report other receptor-targeted SLN imaging agents. Zhi Yang, Department of Nuclear Medicine, Beijing Cancer Hospital, No. 52 Rituximab is a chimeric monoclonal antibody against the CD20 Fucheng Rd., Beijing, 100142, China. E-mail: [email protected] antigen presenting on the membrane of pre-B and mature B lym- *Contributed equally to this work. phocytes. It was approved by the Food and Drug Administration in Published online Mar. 16, 2016. COPYRIGHT © 2016 by the Society of Nuclear Medicine and Molecular 1997 to treat B cell non-Hodgkin lymphomas resistant to chemo- Imaging, Inc. therapy regimens (16,17). Considering there are a large number of 1214 THE JOURNAL OF NUCLEAR MEDICINE • Vol. 57 • No. 8 • August 2016 TABLE 1 with daily quality control. Each patient was injected with 37 MBq Quality Control of 99mTc-Rituximab for Clinical Application (1.0 mCi) of 99mTc-rituximab. Parameter QC specification QC result Lymphatic Mapping Protocol Guided by ultrasound, all patients were administered peritumoral Appearance Clear, colorless Pass subcutaneous injections of 99mTc-rituximab (37.0 MBq, 0.5 mL) 2–18 h Volume 0.5–1.0 mL 0.5 mL before biopsy. In lymphoscintigraphy, 3 point sources (0.37 MBq) were put on the surface of the patient to mark the sternal notch, Injection dose 18.5–37 MBq 37 MBq contralateral sternal margin, and metasternum location as references. pH 4.0–8.0 7.0 Planar lymphoscintigraphy was then acquired by a SPECT system Radio–thin-layer .95% .99% (Siemens; E.Cam) with the patient positioned supine in the anterior chromatography view and the ipsilateral lateral view, to determine the location and Radio–high-performance .95% .99% number of SLNs (Supplemental Figs. 4–8). Acquisition parameters liquid chromatography Ethanol ,5% 0 TABLE 2 Endotoxins ,15 EU/mL Pass Clinical Pathologic Characteristics of 100 Breast Cancer Sterility Sterile Pass Patients Specific activity 111 GBq/μmol Pass Characteristic No. of patients Sex B cells presenting in LNs, we hypothesized that radiolabeled rituximab can serve as an effective imaging tool for SLN identi- Female 100 fication. Therefore, in this work rituximab was directly labeled Age (y) with the most widely used SPECT radionuclide, 99mTc. The resul- #50 49 99m tant tracer, Tc-rituxmab, was further evaluated in a large cohort .50 51 of breast cancer patients (total no. of patients 5 2,317). Here the Left or right side breast cancer feasibility, effectiveness, and safety of using 99mTc-rituxmab for clinical imaging of SLN were reported. Left 45 Right 55 MATERIALS AND METHODS Imaging time after injection of tracer – Patients 2 4h 28 The criterion for inclusion and exclusion of patients meets standard 16–18 h 72 SLN biopsy criteria (supplemental materials [available at http://jnm. Primary tumor location snmjournals.org]). The clinical trial was approved by Peking Univer- Upper inner quadrant 26 sity Cancer Hospital & Institute. From July 2005 to June 2011, pa- tients with breast cancer were recruited at Peking University Cancer Lower inner quadrant 7 Hospital & Institute. The patients’ informed consent was obtained Upper outer quadrant 49 before the tests. SLN imaging was performed in 2,317 breast cancer Lower outer quadrant 16 99m patients using Tc-rituximab followed by SLN biopsy to verify the Central portion 2 imaging results. Histopathologic type Radiotracer Preparation Invasive ductal carcinoma 88 99m Tc radiolabeling of rituximab and radio–high-performance liq- Invasive lobular carcinoma 4 uid chromatography analysis was performed as described (Supple- Other 8 mental Figs. 1–3). Briefly, rituximab (10 mg, 70 nmol) was dissolved in 1 mL of phosphate-buffered solution (pH 7.4, 10 mM), and 0.3 mL Clinical T stage of the solution were taken out to react with 25 mL of 10% (V/V) Tis 1 2-mercaptoethanol for 15 min in the dark. The product was then purified T1 25 by a PD-10 column to obtain 2 mL of reduced rituximab, the solution T2 65 was divided into 0.2 mL for each vial, and the samples were stored at 220°C for further use. When radiolabeling was performed, 0.2 mL of T3 9 solution of reduced rituximab was warmed to room temperature and ER/PR/HER2 added to 10 mL of glucoheptonic acid (100 mg/mL), 15 mL of SnCl2 1/1/1 23 99m (1 mg/mL), and 370–470 MBq of Na TcO4. The reaction mixture −/−/1 11 was shaken at room temperature for 10 min. 99mTc-rituximab was 1/−/− or −/1/− or 1/1/− 49 then purified by a PD-10 column. For clinical use, the radiochemical purity of the tracer was always . 99% tested by radio–thin-layer 1/−/1 or −/1/1 11 chromatography and radio–high-performance liquid chromatography.
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