In-situ x-ray fluorescence imaging of the endogenous iodine distribution in murine thyroids.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
21 02 2022
21 02 2022
Historique:
received:
20
08
2021
accepted:
04
02
2022
entrez:
22
2
2022
pubmed:
23
2
2022
medline:
16
3
2022
Statut:
epublish
Résumé
X-ray fluorescence imaging (XFI) is a non-invasive detection method of small quantities of elements, which can be excited to emit fluorescence x-ray photons upon irradiation with an incident x-ray beam. In particular, it can be used to measure nanoparticle uptake in cells and tissue, thus making it a versatile medical imaging modality. However, due to substantially increased multiple Compton scattering background in the measured x-ray spectra, its sensitivity severely decreases for thicker objects, so far limiting its applicability for tracking very small quantities under in-vivo conditions. Reducing the detection limit would enable the ability to track labeled cells, promising new insights into immune response and pharmacokinetics. We present a synchrotron-based approach for reducing the minimal detectable marker concentration by demonstrating the feasibility of XFI for measuring the yet inaccessible distribution of the endogenous iodine in murine thyroids under in-vivo conform conditions. This result can be used as a reference case for the design of future preclinical XFI applications as mentioned above.
Identifiants
pubmed: 35190621
doi: 10.1038/s41598-022-06786-4
pii: 10.1038/s41598-022-06786-4
pmc: PMC8861059
doi:
Substances chimiques
Iodine
9679TC07X4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2903Informations de copyright
© 2022. The Author(s).
Références
Sanchez-Cano, C. et al. X-ray-based techniques to study the nano-bio interface. ACS Nano 15, 3754–3807 (2021).
pubmed: 33650433
pmcid: 7992135
doi: 10.1021/acsnano.0c09563
Kahl, H. et al. Feasibility of monitoring tumor response by tracking nanoparticle-labelled T cells using X-ray fluorescence imaging—A numerical study. Int. J. Mol. Sci. 22, 8736 (2021).
pubmed: 34445443
pmcid: 8395984
doi: 10.3390/ijms22168736
Endres, P. J., Macrenaris, K. W., Vogt, S., Allen, M. J. & Meade, T. J. Quantitative imaging of cell-permeable magnetic resonance contrast agents using x-ray fluorescence. Mol. Imaging 5, 485–497 (2006).
pubmed: 17150161
doi: 10.2310/7290.2006.00026
Fahrni, C. J. Biological applications of X-ray fluorescence microscopy: Exploring the subcellular topography and speciation of transition metals. Curr. Opin. Chem. Biol. 11, 121–127 (2007).
pubmed: 17353139
doi: 10.1016/j.cbpa.2007.02.039
Chen, H., Rogalski, M. M. & Anker, J. N. Advances in functional X-ray imaging techniques and contrast agents. Phys. Chem. Chem. Phys. PCCP 14, 13469–13486 (2012).
pubmed: 22962667
doi: 10.1039/c2cp41858d
Manohar, N. et al. High-sensitivity imaging and quantification of intratumoral distributions of gold nanoparticles using a benchtop x-ray fluorescence imaging system. Opt. Lett. 44, 5314–5317 (2019).
pubmed: 31674996
pmcid: 7041486
doi: 10.1364/OL.44.005314
Pelaz, B. et al. Diverse applications of nanomedicine. ACS Nano 11, 2313–2381 (2017).
pubmed: 28290206
pmcid: 5371978
doi: 10.1021/acsnano.6b06040
Santibáñez, M., Saavedra, R., Vedelago, J., Malano, F. & Valente, M. Optimized EDXRF system for simultaneous detection of gold and silver nanoparticles in tumor phantom. Radiat. Phys. Chem. 165, 108415 (2019).
doi: 10.1016/j.radphyschem.2019.108415
Schmutzler, O. et al. X-ray fluorescence uptake measurement of functionalized gold nanoparticles in tumor cell microsamples. Int. J. Mol. Sci. 22, 3691 (2021).
pubmed: 33916283
pmcid: 8037401
doi: 10.3390/ijms22073691
Manohar, N., Reynoso, F. J., Diagaradjane, P., Krishnan, S. & Cho, S. H. Quantitative imaging of gold nanoparticle distribution in a tumor-bearing mouse using benchtop x-ray fluorescence computed tomography. Sci. Rep. 6, 22079 (2016).
pubmed: 26912068
pmcid: 4766520
doi: 10.1038/srep22079
Larsson, J. et al. High-spatial-resolution X-ray fluorescence tomography with spectrally matched nanoparticles. Phys. Med. Biol. 63, 164001 (2018).
pubmed: 30033936
doi: 10.1088/1361-6560/aad51e
Grüner, F. et al. Localising functionalised gold-nanoparticles in murine spinal cords by X-ray fluorescence imaging and background-reduction through spatial filtering for human-sized objects. Sci. Rep. 8, 16561 (2018).
pubmed: 30410002
pmcid: 6224495
doi: 10.1038/s41598-018-34925-3
Zhang, S. et al. Quantitative imaging of Gd nanoparticles in mice using benchtop cone-beam X-ray fluorescence computed tomography system. Int. J. Mol. Sci. 20, 2315 (2019).
pmcid: 6539452
doi: 10.3390/ijms20092315
Jung, S. et al. Dynamic in vivo X-ray fluorescence imaging of gold in living mice exposed to gold nanoparticles. IEEE Trans. Med. Imaging 39, 526–533 (2020).
pubmed: 31380749
doi: 10.1109/TMI.2019.2932014
Shaker, K. et al. Longitudinal in-vivo X-Ray fluorescence computed tomography with molybdenum nanoparticles. IEEE Trans. Med. Imaging 39, 3910–3919 (2020).
pubmed: 32746133
doi: 10.1109/TMI.2020.3007165
Krenkel, M. et al. Phase-contrast zoom tomography reveals precise locations of macrophages in mouse lungs. Sci. Rep. 5, 9973 (2015).
pubmed: 25966338
pmcid: 4428069
doi: 10.1038/srep09973
Pittet, M. J. et al. In vivo imaging of T cell delivery to tumors after adoptive transfer therapy. Proc. Natl. Acad. Sci. U. S. A. 104, 12457–12461 (2007).
pubmed: 17640914
pmcid: 1941490
doi: 10.1073/pnas.0704460104
Sanz-Ortega, L., Portilla, Y., Pérez-Yagüe, S. & Barber, D. F. Magnetic targeting of adoptively transferred tumour-specific nanoparticle-loaded CD8
doi: 10.1186/s12951-019-0520-0
Xia, Q. et al. Size- and cell type-dependent cellular uptake, cytotoxicity and in vivo distribution of gold nanoparticles. Int. J. Nanomed. 14, 6957–6970 (2019).
doi: 10.2147/IJN.S214008
Oh, J. M. et al. Development of an athyroid mouse model using 131I ablation after preparation with a low-iodine diet. Sci. Rep. 7, 13284 (2017).
pubmed: 29038462
pmcid: 5643325
doi: 10.1038/s41598-017-13772-8
Li, Y. et al. Quantification of radioactivity by planar gamma-camera images, a promoted method of absorbed dose in the thyroid after iodine-131 treatment. Sci. Rep. 8, 10167 (2018).
pubmed: 29977082
pmcid: 6033874
doi: 10.1038/s41598-018-28571-y
Ke, C.-C. et al. Quantitative measurement of the thyroid uptake function of mouse by Cerenkov luminescence imaging. Sci. Rep. 7, 5717 (2017).
pubmed: 28720762
pmcid: 5515839
doi: 10.1038/s41598-017-05516-5
Rocchi, R., Kunavisarut, T., Ladenson, P. & Caturegli, P. Thyroid uptake of radioactive iodine and scintigraphy in mice. Thyroid 16, 705–706 (2006).
pubmed: 16889498
doi: 10.1089/thy.2006.16.705
Beekman, F. J. et al. Towards in vivo nuclear microscopy: Iodine-125 imaging in mice using micro-pinholes. Eur. J. Nucl. Med. Mol. Imaging 29, 933–938 (2002).
pubmed: 12111135
doi: 10.1007/s00259-002-0805-6
Mettivier, G., Montesi, M. C., Lauria, A. & Russo, P. High resolution 125I pinhole SPECT imaging of the mouse thyroid with the MediSPECT small animal CdTe scanner. In 2008 IEEE Nuclear Science Symposium Conference Record 3790–3796 (2008). https://doi.org/10.1109/NSSMIC.2008.4774283
Brandt, M. P. et al. Micro–single-photon emission computed tomography image acquisition and quantification of sodium-iodide symporter-mediated radionuclide accumulation in mouse thyroid and salivary glands. Thyroid 22, 617–624 (2012).
pubmed: 22540327
pmcid: 3358108
doi: 10.1089/thy.2011.0348
Zwarthoed, C. et al. Single-photon emission computed tomography for preclinical assessment of thyroid radioiodide uptake following various combinations of preparative measures. Thyroid 26, 1614–1622 (2016).
pubmed: 27349131
doi: 10.1089/thy.2015.0652
Spetz, J., Rudqvist, N. & Forssell-Aronsson, E. Biodistribution and dosimetry of free 211At, 125I- and 131I- in rats. Cancer Biother. Radiopharm. 28, 657–664 (2013).
pubmed: 23789969
pmcid: 3793652
doi: 10.1089/cbr.2013.1483
Lavado-Autric, R., Calvo, R. M., de Mena, R. M., de Escobar, G. M. & Obregon, M.-J. Deiodinase activities in thyroids and tissues of iodine-deficient female rats. Endocrinology 154, 529–536 (2013).
pubmed: 23142811
doi: 10.1210/en.2012-1727
Badea, C., Drangova, M., Holdsworth, D. & Johnson, G. In vivo small-animal imaging using micro-CT and digital subtraction angiography. Phys. Med. Biol. 53, R319–R350 (2008).
pubmed: 18758005
pmcid: 2663796
doi: 10.1088/0031-9155/53/19/R01
Parkins, C., Fowler, J., Maughan, R. & Roper, M. Repair in mouse lung for up to 20 fractions of X rays or neutrons. Br. J. Radiol. 58, 225–241 (1985).
pubmed: 4063664
doi: 10.1259/0007-1285-58-687-225
Boone, J. M., Velazquez, O. & Cherry, S. R. Small-animal X-ray dose from micro-CT. Mol. Imaging 3, 149–158 (2004).
pubmed: 15530250
doi: 10.1162/1535350042380326
Falkenberg, G. et al. CRL optics and silicon drift detector for P06 microprobe experiments at 35 keV. Powder Diffr. 35, S34–S37 (2020).
doi: 10.1017/S0885715620000536
Klein, O. & Nishina, Y. Über die Streuung von Strahlung durch freie Elektronen nach der neuen relativistischen Quantendynamik von Dirac. Z. Für Phys. 52, 853–868 (1929).
doi: 10.1007/BF01366453
Tango Controls website. https://www.tango-controls.org
Crawford, A. M. et al. A comparison of parametric and integrative approaches for X-ray fluorescence analysis applied to a Stroke model. J. Synchrotron Radiat. 25, 1780–1789 (2018).
pubmed: 30407190
pmcid: 6225743
doi: 10.1107/S1600577518010895
Schoonjans, T. et al. The xraylib library for X-ray–matter interactions. Recent developments. Spectrochim. Acta Part B At. Spectrosc. 66, 776–784 (2011).
doi: 10.1016/j.sab.2011.09.011
Punzi, G. Sensitivity of searches for new signals and its optimization. eConf C030908, MODT002 (2003).
Brown, T. A. D. et al. Dose-response curve of EBT, EBT2, and EBT3 radiochromic films to synchrotron-produced monochromatic x-ray beams: EBT, EBT2, and EBT3 response to monochromatic x-rays. Med. Phys. 39, 7412–7417 (2012).
pubmed: 23231291
doi: 10.1118/1.4767770
Midgley, S., Schleich, N., Merchant, A. & Stevenson, A. CT dosimetry at the Australian synchrotron for 25–100keV photons and 35–160mm-diameter biological specimens. J. Synchrotron Radiat. 26, 517–527 (2019).
pubmed: 30855263
doi: 10.1107/S1600577518018015
Ziros, P. G. et al. Mice hypomorphic for Keap1, a negative regulator of the Nrf2 antioxidant response, show age-dependent diffuse goiter with elevated thyrotropin levels. Thyroid 31, 23–35 (2021).
pubmed: 32689903
pmcid: 7840308
doi: 10.1089/thy.2020.0044
Silverstein, E. & Bates, R. W. Differences in thyroidal iodine concentration and T/S ratio among strains of mice and rats. Am. J. Physiol. Leg. Content 200, 807–810 (1961).
doi: 10.1152/ajplegacy.1961.200.4.807
Rakov, H. et al. Sex-specific phenotypes of hyperthyroidism and hypothyroidism in aged mice. Biol. Sex Differ. 8, 38 (2017).
pubmed: 29273081
pmcid: 5741944
doi: 10.1186/s13293-017-0159-1