Table 1.
Development stages of [18F]-FDG-PET/CT, [18F]-NaF-PET/CT, [18F]-FES-PET/CT, and [89Zr]-trastuzumab PET/CT
| Checklist | Article | No. of patients | Study type | Scanner | PET measurement | Reference standard | Level of evidence¶ |
|---|---|---|---|---|---|---|---|
| Technical validity* [18F]-FDG-PET (FDA approved) | |||||||
| Repeatability | Van Langen,2012 [5] | 102, 5 studies | Meta-analysis (prospective/retrospective) | PET and PET/CT | Semi-quantitative (SUV) | II | |
| Repeatability | Kramer, 2016 [6] | 9 | Prospective | PET/CT | Semi-quantitative (SUV, TLG, MATV) | III | |
| Repeatability | Weber, 2015 [7] | 74 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability | Rockall, 2016 [8] | 21 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability | Fraum, 2019 [9] | 14 | Prospective | PET/CT | Semi-quantitative (SUV, SUL) | III | |
| Repeatability | Frings, 2014 [10] | 34 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability | Hoang, 2013 [11] | 17 | Prospective | PET/CT | Semi-quantitative ((Δ)SUV) | III | |
| Repeatability | Van Velden, 2014 [12] | 29 | Prospective | PET/CT | Semi-quantitative (SUV, TLG) | III | |
| Reproducibility | Kurland, 2019 [13] | 23 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Reproducibility | Goh, 2012 [14] | 25 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability/reproducibility | Heijmen, 2012 [15] | 20 | Prospective | PET/CT | Semi-quantitative (SUV, TLG, volume) | III | |
| Repeatability/reproducibility | Kolinger, 2019 [16] | 10 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability/reproducibility | Rasmussen, 2015 [17] | 30 | Prospective | PET/CT | Semi-quantitative (SUV, MTV, TLG) | III | |
| Technical validity* [18F]-NaF-PET (FDA approved) | |||||||
| Repeatability | Lin, 2016 [18] | 35 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Repeatability | Wassberg, 2017 [19] | 10 | Prospective | PET/CT | Visual and semi-quantitative (SUV, FTV, TLF) | III | |
| Repeatability | Kurdziel, 2012 [20] | Subgroup of 21 | Prospective | PET/CT | Semi-quantitative (SUV) | III | |
| Reproducibility | Zacho, 2019 [21] | 219 | Prospective | PET/CT | Visual | III | |
| Technical validity* [18F]-FES-PET | |||||||
| Reproducibility | Chae, 2019 [22••] | 90 | Prospective | PET/CT | Visual | III | |
| Technical validity† [89Zr]-trastuzumab-PET: no data are available | |||||||
| Clinical validity† [18F]-FDG-PET (FDA approved) | |||||||
| Diagnosis - primary tumor | Bertagna, 2013 [23] | NR, 13 studies | Meta-analysis (prospective/retrospective) | PET and PET/CT | NR | Partly based on pathology | II |
| Diagnosis - primary tumor | Zhang, 2018 [24•] | 2890, 39 studies | Meta-analysis (NR) | PET and PET/CT | NR | Pathology | II |
| Diagnosis - axillary nodes | Cooper, 2011 [25] | 2591, 26 studies | Meta-analysis (prospective/ retrospective) | PET and PET/CT | Visual | SLNB, ALND | II |
| Diagnosis - axillary nodes | Liang, 2016 [26•] | 1887, 21 studies | Meta-analysis (prospective/retrospective) | PET/CT | Semi-quantitative (SUV) | Fine needle aspiration biopsy, SLNB, ALND | II |
| Diagnosis - axillary nodes | Pritchard, 2012 [27] | 325 | Prospective | PET and PET/CT | Visual | SLNB, ALND | III |
| Diagnosis - recurrence | Xiao, 2016 [28] | 1752, 26 studies | Meta-analysis (prospective/retrospective) | PET and PET/CT | Visual | Pathology, clinical or imaging | II |
| Diagnosis - metastases | Hong, 2013 [29] | 748, 8 studies | Meta-analysis (prospective/retrospective) | PET/CT | Visual, semi-quantitative (not specified) | Pathology, clinical or imaging | II |
| Diagnosis - bone metastases | Rong, 2013 [30] | 668, 7 studies | Meta-analysis (prospective/retrospective) | PET/CT | Visual, semi-quantitative (not specified) | Pathology, clinical, or imaging | II |
| Prognosis - clinicopathological | Groheux, 2011 [31] | 131 | Prospective | PET/CT | Semi-quantitative (SUV) | Pathology | III |
| Prognosis - survival | Diao, 2018 [32•] | 3574, 15 studies | Meta-analysis (prospective/retrospective) | PET and PET/CT | Semi-quantitative (SUV) | Not specified | II |
| Prognosis - survival | Evangelista, 2017 [33] | 275 | Prospective | PET/CT | Visual, semi-quantitative (SUV) | Pathology or imaging | III |
| Prognosis - survival | Zhang, 2013 [34] | 244 | Prospective | PET/CT | Semi-quantitative (SUV) | Pathology, clinical, or imaging | III |
| Therapy response - neoadjuvant | Liu, 2015 [35] | 382, 6 studies | Meta-analysis (prospective/retrospective) | PET/CT | Semi-quantitative (ΔSUV) | Pathology | II |
| Therapy response - neoadjuvant | Tian, 2017 [36•] | 1119, 22 studies | Meta-analysis (prospective/retrospective) | PET/CT | Semi-quantitative (ΔSUV) | Pathology | II |
| Therapy response - neoadjuvant | Coudert, 2014 [37] | 142 | Randomized, prospective | PET/CT | Semi-quantitative (SUV) | Pathology | II |
| Clinical validity† [18F]-NaF-PET (FDA approved) | |||||||
| Diagnosis | Withofs, 2011 [38] | 24 | Prospective | PET/CT | Visual | MRI or CT | III |
| Diagnosis | Damle, 2013 [39] | 72 | Prospective | PET/CT | Visual | Pathology or imaging | III |
| Diagnosis | Liu, 2019 [40•] | Subgroup of 125 (3 studies) | Meta-analyses (prospective/retrospective) | PET/CT | Visual | Pathology, clinical, or imaging | II |
| Prognosis - survival | Peterson, 2018 [41] | 28 | Prospective | PET/CT | Semi-quantitative ((Δ)SUV) | Not specified | III |
| Therapy response | Azad, 2019 [42] | 12 | Prospective | PET/CT | Semi-quantitative ((Δ)metabolic flux, SUV) | Clinical or imaging | III |
| Therapy response | Azad, 2019 [43] | 16 | Prospective | PET/CT | Semi-quantitative ((Δ)SUV, TLM, MTV, SD, entropy, uniformity, kurtosis, skewness) | Clinical or imaging | III |
| Therapy response | Azad, 2019 [44] | 22 | Prospective | PET/CT | Semi-quantitative (ΔSUV) | Clinical or imaging | III |
| Clinical validity† [18F]-FES-PET | |||||||
| Diagnosis | Evangelista, 2016 [45] | 238, 9 studies | Meta-analysis (prospective/retrospective) | PET and PET/CT | Semi-quantitative (SUV) | Partly based on pathology | II |
| Diagnosis | Chae, 2019 [22••] | 90 | Prospective | PET/CT | Visual and semi-quantitative (SUV) | Pathology | III |
| Diagnosis | Venema, 2017 [46] | 13 | Prospective | PET/CT | Semi-quantitative (SUV) | Pathology | III |
| Diagnosis | Gupta, 2017 [47] | 10 | Prospective | PET/CT | Visual and semi-quantitative (SUV) | Pathology | III |
| Prognosis | Kurland, 2017 [48] | 90 | Prospective | PET and PET/CT | Visual and semi-quantitative (SUV, SUL) | Clinical or imaging | III |
| Therapy response | Evangelista, 2016 [45] | 183, 6 studies | Meta-analysis (prospective) | PET and PET/CT | Semi-quantitative (SUV) | Clinical or imaging | II |
| Therapy response | Chae, 2017 [49•] | 26 | Randomized, prospective | PET/CT | Semi-quantitative (SUV) | Pathology | II |
| Therapy response | Van Kruchten, 2015 [50] | 19 | Prospective | PET/CT | Semi-quantitative (SUV) | Clinical or imaging | III |
| Therapy response | Park, 2016 [51] | 24 | Prospective | PET/CT | Semi-quantitative (SUV) | Pathology, clinical, or imaging | III |
| Therapy response | Gong, 2017 [52] | 22 | Prospective | PET/CT | Semi-quantitative ((Δ)SUV) | Imaging | III |
| Clinical validity† [89Zr]-trastuzumab-PET | |||||||
| Diagnosis | Dehdashti, 2018 [53] | 51 | Prospective | PET/CT | Visual and semi-quantitative (SUV) | Pathology, clinical or imaging | III |
| Therapy response | Gebhart, 2016 [54] | 56 | Prospective | PET/CT | Visual and semi-quantitative (SUV) | [18F]-FDG-PET | III |
| Clinical utility† [18F]-FDG-PET (FDA approved) | |||||||
| Cost-effectiveness | Koleva-Kolarova, 2015 [55] | 5073 | Computer simulation | PET/CT | Costs and ICER | § | |
| Clinical utility† [18F]-NaF-PET (FDA approved): no data are available | |||||||
| Clinical utility† [18F]-FES-PET | |||||||
| Cost-effectiveness | Koleva-Kolarova, 2015 [55] | 5073 | Computer simulation | PET/CT | Costs and ICER | § | |
| Cost-effectiveness | Koleva-Kolarova, 2018 [56] | Hypothetical cohort of 1000 | Computer simulation | PET/CT | Costs, LYG and ICER | § | |
| Clinical utility† [89Zr]-trastuzumab-PET | |||||||
| Cost-effectiveness | Koleva-Kolarova, 2018 [56] | Hypothetical cohort of 1000 | Computer simulation | PET/CT | Costs, LYG, and ICER | § | |
Articles are included if they met in- (prospective study design) and exclusion criteria (trials using PET only scanners or including less than 10 (breast cancer) patients (except clinical validity [18F]-FDG-PET ≥ 100 breast cancer patients)
PET positron emission tomography, CT computed tomography, NR not reported, SUV standardized uptake value, TLG total lesion glycolysis, MATV metabolic active tumor volume, SUL SUV normalized by lean body mass, MTV metabolic tumor volume, TLM total lesion metabolism, FTV functional tumor volume, TLF skeletal tumor burden, SLNB sentinel lymph node biopsy, ALND axillary lymph node dissection, SD standard deviation, QALY quality-adjusted life year, ICER incremental cost-effectiveness ratio, LYG life years gained
¶According to ESMO guidelines (I: large randomized trials of good methodological quality or meta-analyses of randomized trials, II: (small) randomized trials or meta-analyses of (small) trials, III: prospective studies, IV: retrospective studies, V: expert opinion) [57]
§Level of evidence does not fit the ESMO criteria
*The study can be performed in various solid tumors, not necessarily breast cancer. Repeatability: refers to measurements performed multiple times in the same subject using the same equipment, software and observers over a short timeframe. Reproducibility: refers to measurements performed using different equipment, different software or observers, or at different sites and times, either in the same or in different subjects
†Always performed in breast cancer patients