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Neodymium doped lanthanide fluoride nanoparticles as contrast agents for luminescent bioimaging and X-ray computed tomography
Nanopartículas de fluoruro de lantano dopadas con neodimio como agentes de contraste para bioimagen mediante luminiscencia y tomografía computarizada de rayos X
Daniel González-Manceboa, Ana I. Becerroa, Roxana M. Calderón-Olveraa, Eugenio Cantelarb, Ariadna Corralc,d, Marcin Balcerzykc,d, Jesús M. de la Fuentee, Manuel Ocañaa,
Corresponding author
mjurado@icmse.csic.es

Corresponding author.
a Instituto de Ciencia de Materiales de Sevilla (CSIC-US), c/Américo Vespucio, 49, 41092 Seville, Spain
b Depto. Física de Materiales, Universidad Autónoma de Madrid, c/Francisco Tomás y Valiente no. 7, 28049 Madrid, Spain
c Centro Nacional de Aceleradores (Universidad de Sevilla-CSIC-Junta de Andalucía), c/Thomas Alva Edison 7, 41092 Sevilla, Spain
d Departamento de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de Sevilla, Avenida Sánchez Pizjuán 4, 41009 Sevilla, Spain
e Instituto de Nanociencia y Materiales de Aragón, CSIC/University of Zaragoza, and CIBER-BBN, Edificio I+D, c/Mariano Esquillor s/n, 50018 Zaragoza, Spain
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anti-counterfeiting <a class="elsevierStyleCrossRef" href="#bib0150">&#91;3&#93;</a>&#44; sensing <a class="elsevierStyleCrossRefs" href="#bib0155">&#91;4&#44;5&#93;</a>&#44; thermometry <a class="elsevierStyleCrossRefs" href="#bib0165">&#91;6&#44;7&#93;</a>&#44; therapy <a class="elsevierStyleCrossRefs" href="#bib0175">&#91;8&#8211;10&#93;</a>&#44; bioimaging <a class="elsevierStyleCrossRefs" href="#bib0190">&#91;11&#8211;13&#93;</a> and theranosis <a class="elsevierStyleCrossRef" href="#bib0205">&#91;14&#93;</a>&#46; For the latter application&#44; the Nd<span class="elsevierStyleSup">3&#43;</span>&#58;LaF<span class="elsevierStyleInf">3</span> system is of particular interest since the excitation &#40;&#8764;800<span class="elsevierStyleHsp" style=""></span>nm&#41; and main emission &#40;&#8764;1060<span class="elsevierStyleHsp" style=""></span>nm&#41; wavelength of the Nd<span class="elsevierStyleSup">3&#43;</span> cations lie in the near-infrared &#40;NIR&#41; region within the so-called biological window I &#40;650&#8211;950<span class="elsevierStyleHsp" style=""></span>nm&#41; and II &#40;1000&#8211;1350<span class="elsevierStyleHsp" style=""></span>nm&#41;&#44; respectively&#44; in which undesired effects such as absorption and scattering of radiation by tissues are minimized and the radiation penetration depth is high <a class="elsevierStyleCrossRef" href="#bib0210">&#91;15&#93;</a>&#46; It is also worth mentioning that X-ray computed tomography &#40;CT&#41; is a powerful imaging technique used in biomedical diagnosis that frequently requires the use of contrast agents &#40;CAs&#41;&#46; CT contrast increases with increasing atomic number &#40;<span class="elsevierStyleItalic">Z</span>&#41; of the elements that make up the CA <a class="elsevierStyleCrossRef" href="#bib0215">&#91;16&#93;</a>&#46; The main CT CAs used nowadays are compounds based on iodine &#40;<span class="elsevierStyleItalic">Z</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>53&#41; and barium &#40;<span class="elsevierStyleItalic">Z</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>56&#41;&#44; which show lower <span class="elsevierStyleItalic">Z</span> values than any lanthanide element &#40;from 57 to 71&#41;&#46; Therefore&#44; Nd-doped LaF<span class="elsevierStyleInf">3</span> might behave as a dual probe for both&#44; luminescent bioimaging and CT&#46; The use of this kind of dual probes would avoid the administration of different&#44; specific CAs for each technique thus minimizing their possible adverse effects&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">It is important to note that particulate CAs for <span class="elsevierStyleItalic">in vivo</span> biomedical applications must meet some specific requirements <a class="elsevierStyleCrossRefs" href="#bib0220">&#91;17&#44;18&#93;</a>&#46; First&#44; the particles must present a uniform size between 20 and 100<span class="elsevierStyleHsp" style=""></span>nm to avoid embolism and the nanoparticles &#40;NPs&#41; premature elimination&#44; since smaller NPs are quickly eliminated through the kidney and larger NPs&#44; by the mononuclear phagocyte system&#46; Second&#44; NPs aggregation in the physiological environment should be avoided to meet the above size criteria&#44; and finally&#44; it is obvious that the NPs must be biocompatible &#40;lack of cytotoxicity&#41;&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Up to now&#44; several procedures have been developed to synthesize Nd<span class="elsevierStyleSup">3&#43;</span> doped LaF<span class="elsevierStyleInf">3</span> NPs&#44; most of which are based on wet chemistry routes&#44; specifically&#44; hydrothermal&#47;solvothermal methods in the absence <a class="elsevierStyleCrossRefs" href="#bib0190">&#91;11&#44;19&#93;</a> or the presence <a class="elsevierStyleCrossRefs" href="#bib0195">&#91;12&#44;20&#8211;23&#93;</a> of organic additives acting as capping or dispersing agents&#46; Among these methods&#44; only that reported by Cheng et al&#46; <a class="elsevierStyleCrossRef" href="#bib0175">&#91;8&#93;</a>&#44; based on the use of oleic acid &#40;OA&#41; as a capping agent succeeded in producing uniform NPs&#46; However&#44; they presented hydrophobic character&#44; as a consequence of the presence of OA moieties on the NPs surface&#44; which precludes their use for bioapplications&#46; Therefore&#44; the search for synthesis procedures yielding monodisperse Nd&#58;LaF<span class="elsevierStyleInf">3</span> NPs colloidally stable in physiological media is still challenging&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">In this paper&#44; a very simple room temperature procedure is reported&#44; which produces uniform and hydrophilic NPs colloidally stable in saline medium&#46; The luminescent properties of these NPs are evaluated as a function of the Nd doping level to find the most efficient phosphor&#46; The X-ray attenuation properties of this system are also analyzed in comparison with a commercial CT CA for the first time in literature&#46; Finally&#44; cytotoxicity experiments are also shown aiming to investigate the suitability of the here reported Nd&#58;LaF<span class="elsevierStyleInf">3</span> NPs for luminescent and CT bioimaging&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Experimental</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Reagents</span><p id="par0025" class="elsevierStylePara elsevierViewall">Ethylene glycol &#40;anhydrous&#44; Sigma Aldrich&#44; 99&#46;8&#37;&#41;&#44; lanthanum nitrate &#40;La&#40;NO<span class="elsevierStyleInf">3</span>&#41;<span class="elsevierStyleInf">3</span>&#183;6H<span class="elsevierStyleInf">2</span>O&#44; Sigma Aldrich&#44; 99&#37;&#41;&#44; neodymium nitrate &#40;Nd&#40;NO<span class="elsevierStyleInf">3</span>&#41;<span class="elsevierStyleInf">3</span>&#183;6H<span class="elsevierStyleInf">2</span>O&#44; Sigma Aldrich&#44; 99&#46;9&#37;&#41;&#44; sodium tetrafluoroborate &#40;NaBF<span class="elsevierStyleInf">4</span>&#44; Sigma Aldrich&#44; 98&#37;&#41;&#44; Iohexol &#40;Sigma Aldrich&#44; analytical standard&#44; &#8805;95&#37;&#41; and saline medium &#40;physiological serum 0&#46;9&#37; NaCl&#44; B&#46; Braun 250<span class="elsevierStyleHsp" style=""></span>mL&#41; were used as received&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Synthesis of nanoparticles</span><p id="par0030" class="elsevierStylePara elsevierViewall">Nd-doped LaF<span class="elsevierStyleInf">3</span> NPs were synthesized following a method similar to that previously developed by us for the synthesis of europium&#8211;bismuth codoped LaF<span class="elsevierStyleInf">3</span><a class="elsevierStyleCrossRef" href="#bib0200">&#91;13&#93;</a>&#46; Briefly&#44; two different solutions were prepared with magnetic stirring at room temperature for 2<span class="elsevierStyleHsp" style=""></span>h&#46; One of them containing lanthanum and neodymium nitrates in 3<span class="elsevierStyleHsp" style=""></span>mL of an ethylene glycol&#47;water mixture &#40;90&#47;10 by volume&#41;&#44; and the other one containing sodium tetrafluoroborate &#40;0&#46;36<span class="elsevierStyleHsp" style=""></span>mol&#47;dm<span class="elsevierStyleSup">3</span>&#41; dissolved in 3<span class="elsevierStyleHsp" style=""></span>mL of the same solvents mixture&#46; Both solutions were admixed together and kept under stirring for a couple of minutes to achieve a good homogenization and then aged at room temperature for 2<span class="elsevierStyleHsp" style=""></span>h&#46; The final concentration of lanthanides was kept constant &#40;&#91;La&#93;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>&#91;Nd&#93;<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;1<span class="elsevierStyleHsp" style=""></span>mol&#47;dm<span class="elsevierStyleSup">3</span>&#41; and the Nd&#47;&#40;La<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>Nd&#41; mol&#37; was varied from 0&#46;25&#37; to 2&#46;0&#37;&#46; The resulting suspension was centrifuged and the precipitates washed&#44; twice with ethanol and once with double distilled water&#46; The so obtained particles were dispersed in distilled water or dried at 50<span class="elsevierStyleHsp" style=""></span>&#176;C for some analyses&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Characterization techniques</span><p id="par0035" class="elsevierStylePara elsevierViewall">Transmission electron microscopy &#40;<span class="elsevierStyleItalic">TEM</span>&#44; JEOL2100Plus&#41; was used to examine the shape and size of the nanoparticles&#46; Particle size distributions were obtained from the micrographs by counting several hundreds of particles&#44; using the free software <span class="elsevierStyleItalic">ImageJ</span>&#46; Dynamic light scattering &#40;DLS&#41; was used to obtain additional information about size and colloidal stability of the nanoparticles&#44; both in aqueous and saline solution &#40;0&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;cm<span class="elsevierStyleSup">3</span> of solid&#41;&#46; The experiments were carried out using a Malvern Zetasizer Nano-ZS90 equipment&#44; which was used as well to measure the Zeta potential of the suspensions&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The crystalline structure of the prepared nanoparticles was assessed by X-ray diffraction &#40;XRD&#41; using a Panalytical X&#8217;Pert Pro diffractometer &#40;Cu K&#945;&#41; with an X-Celetor detector over an angular range of 5&#176;<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>2<span class="elsevierStyleItalic">&#952;</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>120&#176; 2<span class="elsevierStyleItalic">&#952;</span>&#44; 0&#46;02&#176; step width&#44; and 600<span class="elsevierStyleHsp" style=""></span>s counting time&#46; Lattice parameters of the LaF<span class="elsevierStyleInf">3</span> crystal structure were calculated using the Rietveld method with the TOPAS software &#40;TOPAS version 4&#46;2&#44; Bruker AXS&#44; 2009&#41;&#46; The parameters refined were&#58; zero of the diffractometer&#44; background coefficients&#44; scale factor&#44; lattice parameters and profile parameters&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The composition of Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles was determined by inductively coupled plasma &#40;ICP&#41; using ICP-AES Horiba Jobin Yvon&#44; Ultima 2 apparatus&#46; Nanoparticles were previously digested with a small amount of hydrochloride acid&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The photoluminescence of the Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles&#44; in powder form&#44; was analyzed by measuring excitation and emission spectra recorded using a CW diode laser &#64; 810<span class="elsevierStyleHsp" style=""></span>nm as excitation source and an ARC monochromator model SPectraPro 500i with an AsGaIN photodiode&#44; to detect fluorescent emission&#46; The powder samples were placed filling a tiny hole &#40;3<span class="elsevierStyleHsp" style=""></span>mm diameter&#41; practiced in an aluminum foil and sandwiched between two microscope slides&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Nd<span class="elsevierStyleSup">3&#43;</span> decay curves for the <span class="elsevierStyleSup">4</span>F<span class="elsevierStyleInf">3&#47;2</span><span class="elsevierStyleHsp" style=""></span>&#8594;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleSup">4</span>I<span class="elsevierStyleInf">11&#47;2</span> transition &#40;at 1056<span class="elsevierStyleHsp" style=""></span>nm&#41; were obtained under pulsed excitation using a MOPO &#64;<span class="elsevierStyleItalic">&#955;</span><span class="elsevierStyleInf">exc</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>810<span class="elsevierStyleHsp" style=""></span>nm with a pulse width of 10<span class="elsevierStyleHsp" style=""></span>ns and 10<span class="elsevierStyleHsp" style=""></span>Hz repetition rate&#46; The curves were averaged by a Tektronix DPO4104B-L digital oscilloscope&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">For the evaluation of the CT contrast efficiency&#44; aqueous dispersions containing different concentration of the Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles and a commercial CT CA &#40;Iohexol&#41; were prepared&#46; Then&#44; an aliquot &#40;200<span class="elsevierStyleHsp" style=""></span>&#956;L&#41; of each suspension&#44; previously stirred for 2<span class="elsevierStyleHsp" style=""></span>min&#44; was placed in a multiwell microplate along with a Milli-Q water sample as reference for calibration&#46; X-ray attenuation measurements were carried out in a NanoSPECT&#47;CT &#40;Bioscan&#41; using the following acquisition parameters&#58; 106<span class="elsevierStyleHsp" style=""></span>mA current for a 75<span class="elsevierStyleHsp" style=""></span>kV voltage&#44; exposure time per projection of 1500<span class="elsevierStyleHsp" style=""></span>ms and 360 projections per rotation&#46; The final length image was 6<span class="elsevierStyleHsp" style=""></span>cm with a total acquisition time of 18<span class="elsevierStyleHsp" style=""></span>min&#46; The image was reconstructed with Vivoquant image processing software &#40;Invicro&#41;&#44; with the exact cone-beam filtered back-projection algorithm and the Shepp Logan 98&#37; filter&#46; Finally&#44; the images were analyzed by PMOD 3&#46;8 software &#40;PMOD Technologies LLC&#41; and a spherical volume of interest &#40;VOIs&#41; of 2<span class="elsevierStyleHsp" style=""></span>mm radius was made within each sample to calculate the X-ray attenuation &#40;in Hounsfield Unit&#44; HU&#41; for each concentration&#46; The final images were represented in a greyscale&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Cell viability was determined using an MTT colorimetric assay&#46; Vero cells were growth in a Dulbecco&#39;s Modified Eagle&#39;s Medium &#40;DMEM&#41; supplemented with a 5&#37; of glutamine &#40;200<span class="elsevierStyleHsp" style=""></span>mM&#41;&#44; 10&#37; fetal bovine serum &#40;FBS&#41;&#44; 5&#37; penicillin &#40;5000<span class="elsevierStyleHsp" style=""></span>units&#47;cm<span class="elsevierStyleSup">3</span>&#41; and streptomycin &#40;5<span class="elsevierStyleHsp" style=""></span>mg&#47;cm<span class="elsevierStyleSup">3</span>&#41;&#44; at 37<span class="elsevierStyleHsp" style=""></span>&#176;C in a 4&#37; CO<span class="elsevierStyleInf">2</span> atmosphere&#46; Vero cells were disposed in a 96-weel culture plates &#40;5000<span class="elsevierStyleHsp" style=""></span>cell&#47;plate&#41; in 0&#46;2<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">3</span> of DMEM medium&#46; The medium was replaced&#44; after 24<span class="elsevierStyleHsp" style=""></span>h&#44; with another 0&#46;2<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">3</span> DMEM medium containing different concentrations of Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles &#40;0&#46;5&#8211;500<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;mm<span class="elsevierStyleSup">3</span>&#41; and a negative control containing no nanoparticles &#40;non-treated cells&#41;&#46; Five replicates were performed per sample&#46; After 24 incubation&#44; the medium was removed and 0&#46;02<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">3</span> of MMT solution &#40;0&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;cm<span class="elsevierStyleSup">3</span> in phosphate-buffered saline &#40;PBS&#41;&#41; was added to each well&#46; Finally&#44; after incubation for 4<span class="elsevierStyleHsp" style=""></span>h formazan salt was dissolved with 0&#46;2<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">3</span> of dimethyl sulfoxide &#40;DMSO&#41; and the absorbance &#40;Abs&#41; was determined at <span class="elsevierStyleItalic">&#955;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>570<span class="elsevierStyleHsp" style=""></span>nm on a microplate reader &#40;Biotek ELX800&#41;&#46; The relative cell viability &#40;&#37;&#41; related to control wells containing cell culture medium without nanoparticles was calculated by &#91;Abs&#93;test&#47;&#91;Abs&#93;control<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>100&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Results and discussion</span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Morphology&#44; size&#44; and colloidal stability of Nd-doped LaF<span class="elsevierStyleInf">3</span> Nanoparticles</span><p id="par0070" class="elsevierStylePara elsevierViewall">As observed in the TEM images shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#44; regardless of the Nd<span class="elsevierStyleSup">3&#43;</span> doping level&#44; all synthesized Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles showed apparent spherical morphology with similar diameter &#40;around 45<span class="elsevierStyleHsp" style=""></span>nm as determined from the histogram included in the figure&#41;&#46; Nevertheless&#44; a deeper observation of such micrographs revealed the presence of some elongated&#44; higher contrast particles with a length similar to the diameter of the spherical particles and a thickness of 20<span class="elsevierStyleHsp" style=""></span>nm&#46; This observation suggests that the samples consist of homogeneous&#44; lenticular shape NPs&#44; most of which were deposited with their rounded face parallel to the grid plane&#44; giving rise to the spherical shapes&#44; whereas some other fell down with that face perpendicular to the grid&#44; leading to the observed elongated shapes&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">DLS plots for all Nd-doped particles were very similar to those shown in <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#44; which correspond to the 2&#37;Nd&#58;LaF<span class="elsevierStyleInf">3</span> sample&#44; taken as a representative example&#46; The hydrodynamic mean diameter obtained in aqueous solution &#40;pH<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#46;4&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41; for this sample was 50<span class="elsevierStyleHsp" style=""></span>nm&#46; This value was very similar to the mean diameter obtained from the TEM image&#44; indicating that the synthesized nanoparticles are well dispersed&#44; probably due to the presence of electrostatic repulsion forces on their surface&#44; as indicated by the high value of zeta potential &#40;&#43;31<span class="elsevierStyleHsp" style=""></span>mV&#41; measured for this sample&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">To obtain information about the colloidal stability of the Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles in physiological media&#44; they were dispersed in saline medium&#46; In this case&#44; the hydrodynamic diameter obtained &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41; was also very similar &#40;57<span class="elsevierStyleHsp" style=""></span>nm&#41; to that obtained from TEM indicating that the NPs were also colloidally stable in saline medium&#46; The Nd&#58;LaF<span class="elsevierStyleInf">3</span> nanoparticles synthesized in this study meet&#44; therefore&#44; one of the most important requirements for their use <span class="elsevierStyleItalic">in vivo</span>&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">X-ray diffraction</span><p id="par0085" class="elsevierStylePara elsevierViewall">In spite of the low preparation temperature&#44; all samples were crystalline as previously observed for the CeF<span class="elsevierStyleInf">3</span> system synthesized by a similar procedure <a class="elsevierStyleCrossRef" href="#bib0255">&#91;24&#93;</a>&#46; As shown in <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#44; the XRD patterns of all Nd-doped nanoparticles present a single set of reflections&#44; which correspond to hexagonal lanthanum trifluoride &#40;PDF 00-032-0483&#41;&#46; This compound crystallizes in space group <span class="elsevierStyleItalic">P</span>&#8722;<span class="elsevierStyleItalic">3c1</span>&#46; The La<span class="elsevierStyleSup">3&#43;</span> cation is located at the center of a trigonal prism&#44; with 6 fluorine atoms at the top and bottom corners and 3 fluorine atoms at the center of the faces&#44; making a total of 9 F atoms coordinating La&#46; The unit cell volume of the Nd&#58;LaF<span class="elsevierStyleInf">3</span> samples obtained with the Rietveld method &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41; showed a linear decrease with increasing Nd content&#46; This result indicates the substitution of Nd<span class="elsevierStyleSup">3&#43;</span> for La<span class="elsevierStyleSup">3&#43;</span> in the LaF<span class="elsevierStyleInf">3</span> hexagonal lattice as the ionic radius of Nd<span class="elsevierStyleSup">3&#43;</span> &#40;1&#46;163<span class="elsevierStyleHsp" style=""></span>&#8491;&#44; in IX coordination&#41; is smaller than that of La<span class="elsevierStyleSup">3&#43;</span> &#40;1&#46;216<span class="elsevierStyleHsp" style=""></span>&#8491;&#44; in IX coordination&#41;&#46; Finally&#44; it is worth noting that the width of the reflections did not appreciably changed with Nd content&#44; indicating a similar crystallinity degree for all doped samples&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Luminescent properties</span><p id="par0090" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>a shows the excitation spectrum of the 2&#37;Nd&#58;LaF<span class="elsevierStyleInf">3</span> NPs recorded by monitoring the emission at 1064<span class="elsevierStyleHsp" style=""></span>nm&#46; The spectra of the other compositions analyzed in this study are qualitatively very similar to this one&#46; This spectrum shows two broad features with maxima at 733<span class="elsevierStyleHsp" style=""></span>nm and 790<span class="elsevierStyleHsp" style=""></span>nm&#44; which correspond to the electronic transitions in the Nd<span class="elsevierStyleSup">3&#43;</span><span class="elsevierStyleItalic">4f</span> shell labeled in the figure&#46; Excitation of the sample at 733<span class="elsevierStyleHsp" style=""></span>nm or 790<span class="elsevierStyleHsp" style=""></span>nm promotes electrons to the <span class="elsevierStyleSup">4</span>F<span class="elsevierStyleInf">7&#47;2</span> and <span class="elsevierStyleSup">4</span>F<span class="elsevierStyleInf">5&#47;2</span> excited states of Nd<span class="elsevierStyleSup">3&#43;</span>&#44; respectively&#44; as shown in the <span class="elsevierStyleItalic">4f</span> energy levels diagram of Nd<span class="elsevierStyleSup">3&#43;</span> in <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>c&#46; The Nd<span class="elsevierStyleSup">3&#43;</span> excited electrons then decay non-radiatively to the <span class="elsevierStyleSup">4</span>F<span class="elsevierStyleInf">3&#47;2</span> energy level from which they transit to the <span class="elsevierStyleSup">4</span>I<span class="elsevierStyleInf">13&#47;2</span>&#44; <span class="elsevierStyleSup">4</span>I<span class="elsevierStyleInf">11&#47;2</span> and <span class="elsevierStyleSup">4</span>I<span class="elsevierStyleInf">9&#47;2</span> states giving rise to the emission of infrared light with maxima at around 1320<span class="elsevierStyleHsp" style=""></span>nm&#44; 1064<span class="elsevierStyleHsp" style=""></span>nm and 900<span class="elsevierStyleHsp" style=""></span>nm&#44; respectively&#46; The most intense emission&#44; as observed in <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>b&#44; is located at 1064<span class="elsevierStyleHsp" style=""></span>nm&#44; which is inside the biological window II&#46; In this figure&#44; an increase of the intensity of the emission spectra of the Nd&#58;LaF<span class="elsevierStyleInf">3</span> samples with increasing Nd doping level can be also observed&#44; which must be attributed to the increase of the amount of Nd<span class="elsevierStyleSup">3&#43;</span> emitting centers&#46; This behavior is more clearly evidenced in <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>d that shows the integrated area under the curve of the emission spectra corresponding to the different Nd-doped LaF<span class="elsevierStyleInf">3</span> samples&#46; Interestingly&#44; such intensity increase was linear only at low Nd contents while a non-linear behavior was observed above 1&#37; Nd&#46; The emission intensity seems to reach its maximum value for a 2&#37;Nd content&#46; This finding is in agreement with previous observations carried out by Chen et al&#46; for Nd-doped LaF<span class="elsevierStyleInf">3</span> nanoparticles synthesized using oleic acid as capping agent <a class="elsevierStyleCrossRef" href="#bib0195">&#91;12&#93;</a>&#46; Such evolution of the emission intensity is consistent with the presence of the well-known concentration quenching effect at high doping levels&#44; when the emitting centers are close enough to each other as to enable energy transfer processes that eventually result in non-radiative emission and subsequent luminescence quenching <a class="elsevierStyleCrossRefs" href="#bib0260">&#91;25&#44;26&#93;</a>&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a> shows the luminescence decay curves recorded at an emission wavelength of 1064<span class="elsevierStyleHsp" style=""></span>nm for the different Nd-doped LaF<span class="elsevierStyleInf">3</span> samples&#46; All curves were successfully fitted to a biexponential decay of the form&#58;<elsevierMultimedia ident="eq0005"></elsevierMultimedia>where <span class="elsevierStyleItalic">I</span>&#40;<span class="elsevierStyleItalic">t</span>&#41; is the luminescence intensity&#44; <span class="elsevierStyleItalic">t</span> is the time after excitation&#44; and <span class="elsevierStyleItalic">&#964;</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">i</span></span> &#40;<span class="elsevierStyleItalic">i</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#44; 2&#41; is the decay time of the <span class="elsevierStyleItalic">i</span>-component&#44; with intensity <span class="elsevierStyleItalic">I</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">i</span></span>&#46; This biexponential behavior has been usually observed for other lanthanide-based nanoparticulate systems <a class="elsevierStyleCrossRefs" href="#bib0200">&#91;13&#44;27&#93;</a> and arises from the presence of emitting centers in two different locations&#44; namely&#44; in the bulk &#40;long component&#41; and close to the NPs surface &#40;short component&#41; where the luminescence quenching by impurities and defects is more probable to occur&#46; <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> presents the fitting parameters obtained from each curve together with the average decay time &#40;&#60;<span class="elsevierStyleItalic">&#964;</span>&#62;&#41; calculated as&#58;<elsevierMultimedia ident="eq0010"></elsevierMultimedia></p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0100" class="elsevierStylePara elsevierViewall">It can be observed that the average decay time gradually decreases with increasing Nd content&#44; the value for the 2&#37;-doped sample being sensibly lower &#40;53<span class="elsevierStyleHsp" style=""></span>&#956;s&#41; than the others &#40;75&#8211;69<span class="elsevierStyleHsp" style=""></span>&#956;s&#41;&#46; This result agrees with previously reported observations <a class="elsevierStyleCrossRef" href="#bib0250">&#91;23&#93;</a> and confirms the concentration quenching behavior suggested by the evolution of the emission intensity vs&#46; Nd doping level described above&#46; In summary&#44; it can be concluded that&#44; although the most efficient sample is 0&#46;25&#37;Nd&#58;LaF<span class="elsevierStyleInf">3</span> because of its highest lifetime value&#44; the most interesting sample from the application point of view is the one doped with 2&#37;Nd as it shows the highest emission intensity&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">X-ray attenuation capacity</span><p id="par0105" class="elsevierStylePara elsevierViewall">The LaF<span class="elsevierStyleInf">3</span> nanoparticles doped with 2&#37;Nd were selected for the X-ray attenuation study for the reason given above&#46; <a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>a shows the CT phantom images of aqueous suspensions with different concentration of 2&#37;Nd&#58;LaF<span class="elsevierStyleInf">3</span> nanoparticles&#46; The images obtained from aqueous solutions with the same concentration of a commercial CT CA &#40;Iohexol&#41; are also plotted in the figure for comparative purposes&#46; It can be observed that the image contrast clearly increases with increasing NPs and Iohexol concentration&#44; indicating the suitability of our NPs as CA for CT&#46; We have also plotted the X-ray attenuation values&#44; in Hounsfield units&#44; obtained after processing the images shown above&#44; versus the concentration of the CA for both the 2&#37;Nd LaF<span class="elsevierStyleInf">3</span> NPs and Iohexol &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>b&#41;&#46; In both cases&#44; the X-ray attenuation increases linearly with increasing CA concentration&#46; However&#44; the slope of the line corresponding to the Nd&#58;LaF<span class="elsevierStyleInf">3</span> NPs is significantly higher &#40;23&#46;5&#41; than that shown by Iohexol &#40;15&#46;3&#41;&#44; which indicates the higher X-ray attenuation capacity of the here developed probe&#46;</p><elsevierMultimedia ident="fig0030"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Cytotoxicity</span><p id="par0110" class="elsevierStylePara elsevierViewall">The cytotoxicity of the Nd&#58;LaF<span class="elsevierStyleInf">3</span> NPs was analyzed by colorimetric MTT assay&#44; following the methodology described in &#8220;Experimental&#8221; section&#44; using Vero cells&#46; The values obtained for cell survival&#44; higher than 70&#37; in all cases &#40;<a class="elsevierStyleCrossRef" href="#fig0035">Fig&#46; 7</a>&#41; indicate that there is no significant cytotoxicity for NPs concentrations up to 0&#46;1<span class="elsevierStyleHsp" style=""></span>mg&#47;cm<span class="elsevierStyleSup">3</span>&#46; This demonstrates that the here developed bimodal probe meets the biocompatibility requirement needed for its application in bioimaging&#46;</p><elsevierMultimedia ident="fig0035"></elsevierMultimedia></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Conclusions</span><p id="par0115" class="elsevierStylePara elsevierViewall">Uniform neodymium-doped lanthanum trifluoride nanoparticles with hydrophilic character have been synthesized at room temperature by a homogeneous precipitation method in an ethylene glycol&#47;water mixed solvent&#46; The doped nanoparticles showed a lenticular shape with mean diameter around 45<span class="elsevierStyleHsp" style=""></span>nm&#44; irrespective of the neodymium doping level&#46; The luminescent properties of the synthesized samples were analyzed as a function of the Nd content to find the optimum phosphor&#46; On excitation with near infrared light &#40;<span class="elsevierStyleItalic">&#955;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>733<span class="elsevierStyleHsp" style=""></span>nm&#41;&#44; all samples displayed intense luminescence within the second biological window&#46; Lifetime measurements revealed that the maximum luminescence efficiency was attained for the most diluted samples &#40;&#8804;1&#37; Nd<span class="elsevierStyleSup">3&#43;</span>&#41; since such magnitude decreased for the heavier doped sample &#40;2&#37;&#41; as a consequence of concentration quenching&#46; Nevertheless&#44; the latter showed the strongest luminescence due to their higher content in luminescent centers&#44; this sample being&#44; therefore&#44; the most interesting one from the application point of view&#46; In addition&#44; the X-ray attenuation capability of this phosphor has been evaluated for the first time in literature finding that it showed better attenuation properties than a commercial computed tomography contrast agent &#40;Iohexol&#41; indicating the superior suitability of the former for such imaging technique&#46; Finally&#44; the obtained nanoparticles were colloidally stable in saline medium and showed a high biocompatibility&#44; meeting the mean requirements for their use in bioimaging applications&#46;</p></span></span>"
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              "titulo" => "Morphology&#44; size&#44; and colloidal stability of Nd-doped LaF Nanoparticles"
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              "titulo" => "X-ray diffraction"
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              "titulo" => "Luminescent properties"
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              "titulo" => "X-ray attenuation capacity"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The synthesis of uniform neodymium-doped lanthanum trifluoride nanoparticles with lenticular shape and a mean diameter around 45<span class="elsevierStyleHsp" style=""></span>nm by using a homogeneous precipitation method is reported&#46; The luminescent properties of the synthesized samples in terms of their emission spectra and emission lifetime are analyzed as a function of the Nd content to find the optimum phosphor and its suitability for luminescent imaging in the second biological window&#46; The X-ray attenuation properties of the optimum phosphor are evaluated to investigate their additional ability as contrast agent for X-ray computed tomography&#46; Finally&#44; the colloidal stability of the obtained nanoparticles in physiological medium and their cytotoxicity are also analyzed to assess their aptness for <span class="elsevierStyleItalic">in vivo</span> bioimaging applications&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">En este trabajo se ha desarrollado un m&#233;todo de s&#237;ntesis de nanopart&#237;culas uniformes de trifluoruro de lantano dopadas con neodimio&#44; con forma lenticular y un di&#225;metro medio en torno a 45<span class="elsevierStyleHsp" style=""></span>nm&#44; basado en un proceso de precipitaci&#243;n homog&#233;nea en medio acuoso&#46; Las propiedades luminiscentes de las muestras sintetizadas en t&#233;rminos de sus espectros de emisi&#243;n y tiempo de vida de las emisiones se han analizado en funci&#243;n del contenido de neodimio &#40;Nd&#41; para determinar el nanof&#243;sforo &#243;ptimo y su idoneidad para la obtenci&#243;n de im&#225;genes luminiscentes en la segunda ventana biol&#243;gica&#46; Asimismo&#44; se han evaluado las propiedades de atenuaci&#243;n de rayos X del nanof&#243;sforo &#243;ptimo para valorar su capacidad adicional como agente de contraste para tomograf&#237;a computarizada de rayos X&#46; Por &#250;ltimo&#44; tambi&#233;n se han analizado la estabilidad coloidal de las nanopart&#237;culas obtenidas en medio fisiol&#243;gico y su citotoxicidad para determinar su aplicabilidad para la obtenci&#243;n de im&#225;genes biol&#243;gicas <span class="elsevierStyleItalic">in vivo</span>&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">TEM micrographs &#40;left&#41; and the corresponding histograms showing size distribution &#40;right&#41; of the LaF<span class="elsevierStyleInf">3</span> nanoparticles doped with different amounts of Nd<span class="elsevierStyleSup">3&#43;</span>&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Experimental XRD patterns of LaF<span class="elsevierStyleInf">3</span> nanoparticles doped with different amounts of Nd<span class="elsevierStyleSup">3&#43;</span>&#46; The hexagonal pattern of LaF<span class="elsevierStyleInf">3</span> &#40;ICDD No&#58; 00-0032-0483&#41; is shown at the bottom in black&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Excitation spectrum of the 2&#37;Nd<span class="elsevierStyleSup">3&#43;</span>-doped LaF<span class="elsevierStyleInf">3</span> sample&#46; &#40;b&#41; Emission spectra of LaF<span class="elsevierStyleInf">3</span> nanoparticles doped with different amounts of Nd<span class="elsevierStyleSup">3&#43;</span>&#46; &#40;c&#41; Nd<span class="elsevierStyleSup">3&#43;</span> electronic energy levels diagram&#46; &#40;d&#41; Integrated area between 850 and 1400<span class="elsevierStyleHsp" style=""></span>nm of the spectra shown in &#40;b&#41; versus Nd<span class="elsevierStyleSup">3&#43;</span> concentration&#46;</p>"
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        "texto" => "<p id="par0120" class="elsevierStylePara elsevierViewall">Financial support was provided by the <span class="elsevierStyleGrantSponsor" id="gs1">Spanish Ministry of Science&#44; Innovation and Universities</span> under grant <span class="elsevierStyleGrantNumber" refid="gs1">RTI2018-094426-B-I00</span> &#40;AEI&#47;FEDER&#44; UE&#41;&#44; the <span class="elsevierStyleGrantSponsor" id="gs2">Spanish Ministry of Science and Innovation</span> under project <span class="elsevierStyleGrantNumber" refid="gs2">PID2019-110632RB-I00</span> and <span class="elsevierStyleGrantSponsor" id="gs3">Fondo Social de la DGA</span> &#40;grupos DGA&#41;&#46; R&#46;M&#46; Calder&#243;n-Olvera thanks CONACYT-770734 postdoctoral grant&#46; This work is dedicated to the memory of Victor M&#46; Orera&#44; a special scientist and a good friend&#46;</p>"
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Article information
ISSN: 03663175
Original language: English
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