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Application of PET Tracers in Molecular Imaging for Breast Cancer

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Application of PET Tracers in Molecular Imaging for Breast Cancer Current Oncology Reports (2020) 22: 85 https://doi.org/10.1007/s11912-020-00940-9 BREAST CANCER (B OVERMOYER, SECTION EDITOR) Application of PET Tracers in Molecular Imaging for Breast Cancer Jorianne Boers1 • Erik F. J. de Vries2 • Andor W. J. M. Glaudemans2 • Geke A. P. Hospers1 • Carolina P. Schröder1 Published online: 6 July 2020 # The Author(s) 2020 Abstract Purpose of Review Molecular imaging with positron emission tomography (PET) is a powerful tool to visualize breast cancer characteristics. Nonetheless, implementation of PET imaging into cancer care is challenging, and essential steps have been outlined in the international “imaging biomarker roadmap.” In this review, we identify hurdles and provide recommendations for implementation of PET biomarkers in breast cancer care, focusing on the PET tracers 2-[18F]-fluoro-2-deoxyglucose ([18F]- FDG), sodium [18F]-fluoride ([18F]-NaF), 16α-[18F]-fluoroestradiol ([18F]-FES), and [89Zr]-trastuzumab. Recent Findings Technical validity of [18F]-FDG, [18F]-NaF, and [18F]-FES is established and supported by international guidelines. However, support for clinical validity and utility is still pending for these PET tracers in breast cancer, due to variable endpoints and procedures in clinical studies. Summary Assessment of clinical validity and utility is essential towards implementation; however, these steps are still lacking for PET biomarkers in breast cancer. This could be solved by adding PET biomarkers to randomized trials, development of imaging data warehouses, and harmonization of endpoints and procedures. Keywords Breast cancer . Molecular imaging . Positron emission tomography . Technical validation . Clinical validation . Clinical utility Introduction NaF)) are incorporated in cancer management guidelines, such as National Comprehensive Cancer Network (NCCN) Over the last decade, there has been an increasing interest in and European Society for Medical Oncology (ESMO). In or- molecular imaging with positron emission tomography (PET), der to improve successful implementation of PET imaging in particular in the field of oncology. PET imaging is a non- biomarkers into clinical practice, it is essential to identify po- invasive tool to obtain qualitative and quantitative whole- tential hurdles. Recently, an international consensus meeting body information of biological processes. Molecular imaging resulted in the “imaging biomarker roadmap,” describing the in breast cancer (BC) is of particular interest, as it can visualize steps of imaging biomarkers towards clinical practice [1••]. In the estrogen receptor (ER), human epidermal growth factor this review, we describe the current status of PET biomarkers receptor 2 (HER2), and proliferation. However, molecular im- for BC, according to this roadmap. We identify specific chal- aging with PET has not been widely adopted in clinical prac- lenges for each tracer individually and make recommenda- tice of BC. Only two radiotracers (2-[18F]-fluoro-2- tions for next steps towards clinical implementation. deoxyglucose ([18F]-FDG) and sodium [18F]-fluoride ([18F]- This article is part of the Topical Collection on Breast Cancer Development Stages of Imaging Biomarkers * Carolina P. Schröder [email protected] The imaging biomarker roadmap describes three parallel 1 tracks, towards biomarker implementation in clinical practice Department of Medical Oncology, University of Groningen, •• University Medical Center Groningen, Hanzeplein 1, 9700 [1 ]. Technical validity, i.e., whether the test can be trusted, RB Groningen, The Netherlands requires harmonization and standardization of techniques as 2 Medical Imaging Center, Department of Nuclear Medicine and an assessment of repeatability and reproducibility. Clinical Molecular Imaging, University of Groningen, University Medical validity, i.e., whether the test is clinically meaningful, ad- Center Groningen, Groningen, The Netherlands dresses the discriminatory value to predict diagnosis, 85 Page 2 of 16 Curr Oncol Rep (2020) 22: 85 prognosis, or therapy response. Finally, clinical utility, i.e., performance, and reproducible assessments [3, 59]. Since whether the test improves patient outcome and is cost-effec- 2010, the number of accredited centers has increased over tive, is determined by health-related measurements. time in Europe and beyond [60]. Successful progress through these tracks is essential for a test to pass from analytical to clinical research stage, and subse- Clinical Validity quently to routine clinical practice [1••]. For [18F]-FDG-PET/CT, we focused on clinical validity stud- ies with at least 100 BC patients. A meta-analysis of 13 studies Search Strategy (see Table 1) reported incidental and unexpected breast uptake detected by [18F]-FDG-PET(/CT) [23]. Overlap between For this literature review, the database PubMed was searched SUVs in malignant and benign breast incidentalomas was until September 2019. PET tracers were included if Food and found, and not all lesions were further histologically exam- Drug Administration (FDA) approved or at least two prospec- ined. Therefore, [18F]-FDG-PET/CT is not routinely used for tive clinical articles, including ≥ 50 BC patients, were pub- diagnosis of primary BC. With regard to diagnosis of axillary lished within the past 5 years. As a result, four radiotracers lymph node metastases in BC, a meta-analysis was performed were selected ([18F]-FDG, [18F]-NaF, 16α-[18F]- of studies comparing [18F]-FDG-PET(/CT) to the reference fluoroestradiol ([18F]-FES), and zirconium-89 [89Zr]- standard: axillary lymph node dissection (ALND) or sentinel trastuzumab). Search terms were repeatability, reproducibili- lymph node biopsy (SLNB) [25]. In 7 out of 26 studies in- ty, inter- and intra-observer, diagnosis, prognosis, response to volving 862 BC patients, [18F]-FDG-PET/CT sensitivity was treatment, survival, metastases, technical and clinical validity/ 56% and specificity 96%, compared to 52% and 95% for utility, cost-effectiveness, BC, PET, and meta-analysis. ALND and/or SLNB [25]. Another meta-analysis (21 studies including 1887 BC patients), using ALND and/or SLNB as reference standard, showed a sensitivity and specificity of Development Stages of [18F]-FDG-PET/CT 64% and 93%, respectively, for detection of axillary lymph node metastases by [18F]-FDG-PET/CT [26•]. Based on these Technical Validity data, [18F]-FDG-PET/CT is not recommended in the EANM, NCCN, or ESMO guidelines for detection of axillary lymph [18F]-FDG-PET/computed tomography (CT) can detect in- node metastases. However, as axillary BC management has creased glucose metabolism in cancer cells and is indicated evolved over the last decades, the use of [18F]-FDG-PET/CT for multiple oncological indications [2, 3]. [18F]-FDG is phos- in this setting may change as well. For instance, according to phorylated by the enzyme hexokinase and trapped inside the Dutch BC guideline, [18F]-FDG-PET/CT can be consid- (tumor) cells [4]. The reproducibility and repeatability of ered for staging of BC patients prior to neoadjuvant chemo- [18F]-FDG-PET/CT were assessed for various cancer types therapy, although a biopsy of axillary lymph nodes with high (see Table 1 for overview) [58]. One meta-analysis of 5 stud- [18F]-FDG uptake is advised to avoid false positive results ies, including 102 cancer patients of which 6 had metastatic [61]. With regard to [18F]-FDG-PET/CT for diagnosis of re- BC (MBC), assessed the repeatability of [18F]-FDG-PET(/ current or distant metastases in BC, two meta-analyses includ- CT) by measuring the standardized uptake value (SUV)max/ ing a total of 2500 patients (2 studies with overlapping sub- mean in the same patient on two separate occasions with an jects) showed both high sensitivity (92–96%) and specificity interval of 1–4days[5]. A high test-retest interclass correla- (82–95%) [28, 29]. For the detection of bone metastases, 18 tion coefficient (ICC) of 0.90 and 0.91 was found for SUVmax [ F]-FDG-PET/CT showed a sensitivity and specificity of and SUVmean, respectively. Reproducibility across different 93% and 99%, versus 81% and 96% respectively, for conven- scannerswasassessedin23patients,17withBC[13]. tional bone scintigraphy, as determined in a meta-analysis Patients underwent two [18F]-FDG-PET/CT scans within involving 668 BC patients in 7 studies [30]. According to 15 days on the same scanner or on different scanners at dif- the EANM, ESMO, and NCCN guidelines, [18F]-FDG-PET/ ferent sites. Cross-calibration of PET/CT scanners and dose CT should be considered in cases of suspected recurrence or calibrator was performed. The average difference in SUVmax equivocal findings on standard imaging and can be used for between test-retest [18F]-FDG-PET/CT, using the same scan- staging in high-risk BC patients [2, 3, 62, 63••, 64, 65••]. ner, was 8% versus 18% on different scanners. International Despite the non-specific uptake of [18F]-FDG, preoperative 18 standardization efforts to improve reproducibility resulted in [ F]-FDG uptake, expressed as SUVmax, was found to be the European Association of Nuclear Medicine (EANM) related to prognostic pathological characteristics assessed on 18 guideline for F imaging procedures, followed in 2010 by core biopsy in primary BC. SUVmax was higher in ER− than the Research Ltd. (EARL) accreditation program to assure ER+ tumors (7.6 versus 5.5); higher uptake was also observed independent quality control, comparable scanner in triple-negative tumors, tumor grade 3, ductal carcinoma, Curr 18 18 18 89 Table 1 Development stages
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