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Performance of Nanoscan PET/CT and PET/MR for Quantitative Chomet et al. EJNMMI Res (2021) 11:57 https://doi.org/10.1186/s13550-021-00799-2 ORIGINAL RESEARCH Open Access Performance of nanoScan PET/CT and PET/ MR for quantitative imaging of 18F and 89Zr as compared with ex vivo biodistribution in tumor-bearing mice Marion Chomet, Maxime Schreurs, Ricardo Vos, Mariska Verlaan, Esther J. Kooijman, Alex J. Poot, Ronald Boellaard, Albert D. Windhorst, Guus AMS van Dongen, Danielle J. Vugts, Marc C. Huisman and Wissam Beaino* Abstract Introduction: The assessment of ex vivo biodistribution is the preferred method for quantifcation of radiotracers biodistribution in preclinical models, but is not in line with current ethics on animal research. PET imaging allows for noninvasive longitudinal evaluation of tracer distribution in the same animals, but systemic comparison with ex vivo biodistribution is lacking. Our aim was to evaluate the potential of preclinical PET imaging for accurate tracer quantif- cation, especially in tumor models. Methods: NEMA NU 4-2008 phantoms were flled with 11C, 68Ga, 18F, or 89Zr solutions and scanned in Mediso nan- oPET/CT and PET/MR scanners until decay. N87 tumor-bearing mice were i.v. injected with either [18F]FDG (~ 14 MBq), kept 50 min under anesthesia followed by imaging for 20 min, or with [89Zr]Zr-DFO-NCS-trastuzumab (~ 5 MBq) and imaged 3 days post-injection for 45 min. After PET acquisition, animals were killed and organs of interest were col- lected and measured in a γ-counter to determine tracer uptake levels. PET data were reconstructed using TeraTomo reconstruction algorithm with attenuation and scatter correction and regions of interest were drawn using Vivoquant software. PET imaging and ex vivo biodistribution were compared using Bland–Altman plots. Results: In phantoms, the highest recovery coefcient, thus the smallest partial volume efect, was obtained with 18F for both PET/CT and PET/MR. Recovery was slightly lower for 11C and 89Zr, while the lowest recovery was obtained with 68Ga in both scanners. In vivo, tumor uptake of the 18F- or 89Zr-labeled tracer proved to be similar irrespective whether quantifed by either PET/CT and PET/MR or ex vivo biodistribution with average PET/ex vivo ratios of 0.8–0.9 and a deviation of 10% or less. Both methods appeared less congruent in the quantifcation of tracer uptake in healthy organs such as brain, kidney, and liver, and depended on the organ evaluated and the radionuclide used. Conclusions: Our study suggests that PET quantifcation of 18F- and 89Zr-labeled tracers is reliable for the evalua- tion of tumor uptake in preclinical models and a valuable alternative technique for ex vivo biodistribution. However, PET and ex vivo quantifcation require fully described experimental and analytical procedures for reliability and reproducibility. *Correspondence: [email protected] Amsterdam UMC, Vrije Universiteit Amsterdam, Radiology & Nuclear Medicine, Cancer Center Amsterdam, De Boelelaan 1117, Amsterdam 1081 HV, The Netherlands © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Chomet et al. EJNMMI Res (2021) 11:57 Page 2 of 11 Keywords: PET-CT, PET-MRI, Preclinical imaging, Quantifcation, Ex vivo biodistribution Introduction and reproducible quantitative PET data in small animals Preclinical positron emission tomography (PET) imaging studies: i. the camera itself (i.e., size, type, and number of has become a crucial tool for the development and evalu- detectors), ii. the physical properties of the PET isotope ation of radiolabeled tracers and therapeutic drugs and used (i.e., positron range), and iii. the animal models and can facilitate faster translation from bench to bedside [1, animal handling. Moreover, preclinical PET studies still 2]. Preclinical PET cameras have been in constant evo- lack standardized protocols that lead to unreliable data lution to ofer improved spatial and temporal resolution making inter-study comparison more challenging. and sensitivity. Nowadays, the advantages of functional In recent publications, the reliability and reproducibil- and anatomical imaging are combined within hybrid ity of preclinical data acquired using phantoms and vari- cameras where computerized tomography (CT), mag- ous cameras in diferent imaging centers were evaluated. netic resonance (MR) or fuorescent imaging technolo- Te key factors that resulted in variability were, apart gies are added to the PET scanners [3, 4]. Compared to from the type of camera used, the diferences in animal CT, MRI ofers better soft tissue resolution and no radia- handling and image acquisition protocols and analysis, tion exposure. However, preclinical and clinical develop- and variability between users [11–13]. ment of PET/MR scanners came with their own specifc PET imaging is rarely used for the quantifcation of technical hurdles due to the strong magnetic feld that radiotracer biodistribution and data that allow compari- might afect PET functionality, making the combination son between in vivo and ex vivo uptake are very scarce. of the PET with MRI components more challenging than Te infuence of the partial volume efect (PVE) is often with CT. Furthermore, as MRI does not provide informa- mentioned as a cause of quantifcation inaccuracy. PVE tion on electron density, the attenuation coefcient map results from the limited spatial resolution of preclinical is more difcult to obtain and can result in lower imaging cameras which impairs accurate measurement of activ- resolution [2]. ity concentrations in small regions surrounded by other To evaluate the potential and in vivo behavior of radi- organs or background activity. Consequently, an under- otracers, ex vivo biodistribution is generally considered estimation of tracer uptake, especially in, e.g., small the method of choice. In such studies, the radiotracer tumors, orthotopic or metastatic models, organs or brain is administered to animals, and at predetermined time sub-regions is observed [10]. points tissues of interest are collected, weighed, and In this study, we evaluated the performance of a Mediso counted for radioactivity. Percentage of injected dose nanoScan PET/CT and PET/MR scanner for tracer quan- (or percentage of activity) per gram of tissue (%ID/g or tifcation in subcutaneous tumors and selected organs by %IA/g) is then calculated providing information about direct comparison of PET imaging with ex vivo biodis- the biodistribution and in vivo kinetics of the PET tracer. tribution. We evaluated the critical parameters involved A large number of animals is usually used for a limited in reliable PET quantifcation in vitro as well as in vivo. number of time points, which is not in line with the ethi- Firstly, phantoms flled with the most commonly used cal aim to reduce animal use. Unlike ex vivo biodistribu- PET radionuclides 11C, 68Ga, 18F, and 89Zr were used in tion, preclinical PET imaging is ofering the possibility order to evaluate the performance of the cameras with for longitudinal studies, where the same animals can respect to linearity, recovery coefcient, PVE and spill- be used as their own control at multiple and early time over efect. Secondly, breast cancer tumor-bearing mice points. Tis fully complies with current ethics on animal were used for quantifcation of [18F]FDG and [89Zr]Zr- experiments and the 3Rs guidelines (Reduction, Replace- DFO-NCS-trastuzumab uptake in tumors and selected ment, Refnement) [5–8]. Furthermore, PET imaging organs (brain, kidney and liver) by PET imaging as well allows quantitative and visual whole body assessment of as by ex vivo biodistribution. Congruency between PET tracer uptake giving insights on the heterogeneity of its quantifcation and ex vivo biodistribution was evaluated distribution often not possible with ex vivo biodistribu- using Bland–Altman plots. tion. Despite the increased availability of preclinical PET cameras in research centers, PET imaging is mostly used Materials and methods as a qualitative visualization tool and not as a replace- Phantom experiments ment for ex vivo quantifcation of biodistribution [9]. All experiments were performed with a Mediso nanoS- Te review of Kuntner and Stout [10] summarized the can PET/CT and Mediso nanoScan PET/MR (Mediso crucial parameters that are needed to obtain reliable Ltd., Hungary) [14]. Two NEMA NU 4–2008 phantoms, Chomet et al. EJNMMI Res (2021) 11:57 Page 3 of 11 18 in conditions similar to those described by others [15– for reliable analysis. In the F study (n = 20), animals 18], were flled with solutions containing either car- were imaged by PET/CT (n 10) or by PET/MR (n 10) = 89 = bon-11 (t1/2 20.4 min, Iß 100%, Eßmax 960 keV, followed by ex vivo biodistribution. In the Zr study 11 = + = = [ C]acetate), gallium-68 (t1/2 67.6 min, Iß 90%, (n 10), animals were imaged by PET/CT and PET/MR 68 = + = = Eßmax 1900 keV, [ Ga]GaCl3 in 0.1 M HCl), fuorine-18 before ex vivo biodistribution. Inclusion and exclusion = 18 (t1/2 109.8 min, Iß 100%, Eßmax 634 keV, [ F]FDG) criteria: time points were decided a priori and corre- = + = = 18 89 or zirconium-89 (t 78.4 h, I 23%, E 897 keV, spond to standard practice with the F and Zr tracers 1/2 = ß+ = ßmax = [89Zr]Zr-DFO-NCS-trastuzumab).
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