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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">X-ray-Induced Shortwave Infrared Biomedical
Imaging Using Rare-Earth Nanoprobes</title><author><name sortKey="Naczynski, Dominik X0a Jan" sort="Naczynski, Dominik X0a Jan" uniqKey="Naczynski D" first="Dominik X0a Jan" last="Naczynski">Dominik X0a Jan Naczynski</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Sun, Conroy" sort="Sun, Conroy" uniqKey="Sun C" first="Conroy" last="Sun">Conroy Sun</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Turkcan, Silvan" sort="Turkcan, Silvan" uniqKey="Turkcan S" first="Silvan" last="Türkcan">Silvan Türkcan</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jenkins, Cesare" sort="Jenkins, Cesare" uniqKey="Jenkins C" first="Cesare" last="Jenkins">Cesare Jenkins</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=" and" id="aff2">Department of Mechanical Engineering</nlm:aff></affiliation></author><author><name sortKey="Koh, Ai Leen" sort="Koh, Ai Leen" uniqKey="Koh A" first="Ai Leen" last="Koh">Ai Leen Koh</name><affiliation><nlm:aff id="aff2">Stanford Nanocharacterization Laboratory,<institution>Stanford University</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Ikeda, Debra" sort="Ikeda, Debra" uniqKey="Ikeda D" first="Debra" last="Ikeda">Debra Ikeda</name><affiliation><nlm:aff id="aff4">Department of Radiology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Pratx, Guillem" sort="Pratx, Guillem" uniqKey="Pratx G" first="Guillem" last="Pratx">Guillem Pratx</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Xing, Lei" sort="Xing, Lei" uniqKey="Xing L" first="Lei" last="Xing">Lei Xing</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25485705</idno><idno type="pmc">4296927</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4296927</idno><idno type="RBID">PMC:4296927</idno><idno type="doi">10.1021/nl504123r</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000069</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000069</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">X-ray-Induced Shortwave Infrared Biomedical
Imaging Using Rare-Earth Nanoprobes</title><author><name sortKey="Naczynski, Dominik X0a Jan" sort="Naczynski, Dominik X0a Jan" uniqKey="Naczynski D" first="Dominik X0a Jan" last="Naczynski">Dominik X0a Jan Naczynski</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Sun, Conroy" sort="Sun, Conroy" uniqKey="Sun C" first="Conroy" last="Sun">Conroy Sun</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Turkcan, Silvan" sort="Turkcan, Silvan" uniqKey="Turkcan S" first="Silvan" last="Türkcan">Silvan Türkcan</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jenkins, Cesare" sort="Jenkins, Cesare" uniqKey="Jenkins C" first="Cesare" last="Jenkins">Cesare Jenkins</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=" and" id="aff2">Department of Mechanical Engineering</nlm:aff></affiliation></author><author><name sortKey="Koh, Ai Leen" sort="Koh, Ai Leen" uniqKey="Koh A" first="Ai Leen" last="Koh">Ai Leen Koh</name><affiliation><nlm:aff id="aff2">Stanford Nanocharacterization Laboratory,<institution>Stanford University</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Ikeda, Debra" sort="Ikeda, Debra" uniqKey="Ikeda D" first="Debra" last="Ikeda">Debra Ikeda</name><affiliation><nlm:aff id="aff4">Department of Radiology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Pratx, Guillem" sort="Pratx, Guillem" uniqKey="Pratx G" first="Guillem" last="Pratx">Guillem Pratx</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Xing, Lei" sort="Xing, Lei" uniqKey="Xing L" first="Lei" last="Xing">Lei Xing</name><affiliation><nlm:aff id="aff1">Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></nlm:aff></affiliation></author></analytic><series><title level="j">Nano Letters</title><idno type="ISSN">1530-6984</idno><idno type="eISSN">1530-6992</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p content-type="toc-graphic"><graphic xlink:href="nl-2014-04123r_0007" id="ab-tgr1"></graphic></p><p>Shortwave infrared (SWIR or NIR-II)
light provides significant advantages for imaging biological structures
due to reduced autofluorescence and photon scattering. Here, we report
on the development of rare-earth nanoprobes that exhibit SWIR luminescence
following X-ray irradiation. We demonstrate the ability of X-ray-induced
SWIR luminescence (X-IR) to monitor biodistribution and map lymphatic
drainage. Our results indicate X-IR imaging is a promising new modality
for preclinical applications and has potential for dual-modality molecular
disease imaging.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Smith, A M" uniqKey="Smith A">A. M. Smith</name></author><author><name sortKey="Mancini, M C" uniqKey="Mancini M">M. C. Mancini</name></author><author><name sortKey="Nie, S" uniqKey="Nie S">S. Nie</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Welsher, K" uniqKey="Welsher K">K. Welsher</name></author><author><name sortKey="Sherlock, S P" uniqKey="Sherlock S">S. P. Sherlock</name></author><author><name sortKey="Dai, H" uniqKey="Dai H">H. Dai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hong, G" uniqKey="Hong G">G. Hong</name></author><author><name sortKey="Lee, J C" uniqKey="Lee J">J. C. Lee</name></author><author><name sortKey="Robinson, J T" uniqKey="Robinson J">J. T. Robinson</name></author><author><name sortKey="Raaz, U" uniqKey="Raaz U">U. Raaz</name></author><author><name sortKey="Xie, L" uniqKey="Xie L">L. Xie</name></author><author><name sortKey="Huang, N F" uniqKey="Huang N">N. F. Huang</name></author><author><name sortKey="Cooke, J P" uniqKey="Cooke J">J. P. Cooke</name></author><author><name sortKey="Dai, H" uniqKey="Dai H">H. Dai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Naczynski, D X0a J" uniqKey="Naczynski D">D.
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Nano Lett</journal-id><journal-id journal-id-type="iso-abbrev">Nano Lett</journal-id><journal-id journal-id-type="publisher-id">nl</journal-id><journal-id journal-id-type="coden">nalefd</journal-id><journal-title-group><journal-title>Nano Letters</journal-title></journal-title-group><issn pub-type="ppub">1530-6984</issn><issn pub-type="epub">1530-6992</issn><publisher><publisher-name>American Chemical Society</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25485705</article-id><article-id pub-id-type="pmc">4296927</article-id><article-id pub-id-type="doi">10.1021/nl504123r</article-id><article-categories><subj-group><subject>Letter</subject></subj-group></article-categories><title-group><article-title>X-ray-Induced Shortwave Infrared Biomedical
Imaging Using Rare-Earth Nanoprobes</article-title></title-group><contrib-group><contrib contrib-type="author" id="ath1"><name><surname>Naczynski</surname><given-names>Dominik
Jan</given-names></name><xref rid="aff1" ref-type="aff">†</xref></contrib><contrib contrib-type="author" id="ath2"><name><surname>Sun</surname><given-names>Conroy</given-names></name><xref rid="aff1" ref-type="aff">†</xref></contrib><contrib contrib-type="author" id="ath3"><name><surname>Türkcan</surname><given-names>Silvan</given-names></name><xref rid="aff1" ref-type="aff">†</xref></contrib><contrib contrib-type="author" id="ath4"><name><surname>Jenkins</surname><given-names>Cesare</given-names></name><xref rid="aff1" ref-type="aff">†</xref><xref rid="aff2" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath5"><name><surname>Koh</surname><given-names>Ai Leen</given-names></name><xref rid="aff2" ref-type="aff">§</xref></contrib><contrib contrib-type="author" id="ath6"><name><surname>Ikeda</surname><given-names>Debra</given-names></name><xref rid="aff4" ref-type="aff">∥</xref></contrib><contrib contrib-type="author" id="ath7"><name><surname>Pratx</surname><given-names>Guillem</given-names></name><xref rid="aff1" ref-type="aff">†</xref></contrib><contrib contrib-type="author" corresp="yes" id="ath8"><name><surname>Xing</surname><given-names>Lei</given-names></name><xref rid="cor1" ref-type="other">*</xref><xref rid="aff1" ref-type="aff">†</xref></contrib><aff id="aff1"><label>†</label>Department of Radiation Oncology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></aff><aff id="aff2"><sup>‡</sup>Department of Mechanical Engineering and<sup>§</sup>Stanford Nanocharacterization Laboratory,<institution>Stanford University</institution>, Palo Alto, California 94305,<country>United States</country></aff><aff id="aff4"><label>∥</label>Department of Radiology,<institution>Stanford University School of Medicine</institution>, Palo Alto, California 94305,<country>United States</country></aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>E-mail: <email>lei@stanford.edu</email>.</corresp></author-notes><pub-date pub-type="pmc-release"><day>08</day><month>12</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>08</day><month>12</month><year>2014</year></pub-date><pub-date pub-type="ppub"><day>14</day><month>01</month><year>2015</year></pub-date><volume>15</volume><issue>1</issue><fpage>96</fpage><lpage>102</lpage><history><date date-type="received"><day>07</day><month>08</month><year>2014</year></date><date date-type="rev-recd"><day>03</day><month>12</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 American
Chemical Society</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>American
Chemical Society</copyright-holder><license><license-p>This is an open access article published under an ACS AuthorChoice <ext-link ext-link-type="uri" xlink:href="http://pubs.acs.org/page/policy/authorchoice_termsofuse.html">License</ext-link>, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.</license-p></license></permissions><abstract><p content-type="toc-graphic"><graphic xlink:href="nl-2014-04123r_0007" id="ab-tgr1"></graphic></p><p>Shortwave infrared (SWIR or NIR-II)
light provides significant advantages for imaging biological structures
due to reduced autofluorescence and photon scattering. Here, we report
on the development of rare-earth nanoprobes that exhibit SWIR luminescence
following X-ray irradiation. We demonstrate the ability of X-ray-induced
SWIR luminescence (X-IR) to monitor biodistribution and map lymphatic
drainage. Our results indicate X-IR imaging is a promising new modality
for preclinical applications and has potential for dual-modality molecular
disease imaging.</p></abstract><kwd-group><kwd>NIR-II</kwd><kwd>SWIR</kwd><kwd>second near-infrared</kwd><kwd>rare-earth</kwd><kwd>imaging</kwd><kwd>X-ray luminescence</kwd></kwd-group><funding-group><funding-statement><funding-source>National Institutes of Health, United States</funding-source></funding-statement></funding-group><custom-meta-group><custom-meta><meta-name>document-id-old-9</meta-name><meta-value>nl504123r</meta-value></custom-meta><custom-meta><meta-name>document-id-new-14</meta-name><meta-value>nl-2014-04123r</meta-value></custom-meta><custom-meta><meta-name>ccc-price</meta-name><meta-value></meta-value></custom-meta></custom-meta-group></article-meta></front><body><p>Shortwave infrared (SWIR, alternatively referred to as NIR-II) imaging
is an emerging optical modality that utilizes light in the second
infrared window (1000–2300 nm) to visualize biological features
with improved resolution and at greater tissue depth when compared
to conventional near-infrared (NIR, 700–1000 nm) imaging approaches.<sup><xref ref-type="bibr" rid="ref1">1</xref>−<xref ref-type="bibr" rid="ref3">3</xref></sup> These benefits have led to growing interest in the development of
biologically benign molecular probes that can harness SWIR.<sup><xref ref-type="bibr" rid="ref4">4</xref>,<xref ref-type="bibr" rid="ref5">5</xref></sup> While nanomaterials including single-wall carbon nanotubes (SWNTs)<sup><xref ref-type="bibr" rid="ref6">6</xref>−<xref ref-type="bibr" rid="ref8">8</xref></sup> and quantum dots (QDs)<sup><xref ref-type="bibr" rid="ref9">9</xref></sup> have been investigated
as SWIR imaging probes, these materials face significant translational
challenges including low quantum efficiency, toxic compositions, and
size-dependent emissions.</p><p>Rare-earth doped nanoprobes (REs)
have recently shown great promise for SWIR molecular imaging.<sup><xref ref-type="bibr" rid="ref4">4</xref></sup> REs are inorganic nanoparticles composed of a
lanthanide doped host material surrounded by a nondoped shell (Figure <xref rid="fig1" ref-type="fig">1</xref>a). These core–shell nanostructured REs exhibit
numerous advantageous imaging properties including exceptional photostability,
tunable emissions with large Stokes shifts (>100 nm), and bright
SWIR luminescence. These SWIR emissions can be induced from REs using
continuous-wave NIR excitation, which has led to growing interest
in the development of imaging approaches that utilize SWIR for biomedical
applications.<sup><xref ref-type="bibr" rid="ref10">10</xref></sup> Previous work has shown
that SWIR exhibits exceptional temporal and spatial resolving capabilities
and can be used for tracking nanoparticle biodistribution, vascular
mapping, and tumor detection.<sup><xref ref-type="bibr" rid="ref4">4</xref></sup></p><fig id="fig1" position="float"><label>Figure 1</label><caption><p>Schematic of
rare-earth doped nanoprobes showing the lanthanide-doped core surrounded
by an undoped shell (a). TEM images of REs reveal spherical morphology
(b). Individual lattice fringes were used to determine a predominantly
hexagonal crystalline phase in the RE population (inset). REs displayed
narrow size distribution as measured by analysis of TEM images (c).
EDS confirmed the presence of the SWIR-emitting Er dopant in the REs
(d).</p></caption><graphic xlink:href="nl-2014-04123r_0002" id="gr1" position="float"></graphic></fig><p>We have recently shown that X-rays
are capable of exciting the luminescent centers of various nanomaterials.<sup><xref ref-type="bibr" rid="ref11">11</xref>,<xref ref-type="bibr" rid="ref12">12</xref></sup> In particular, X-ray irradiation of fluorescent nanomaterials such
as metal–organic frameworks,<sup><xref ref-type="bibr" rid="ref13">13</xref></sup> gold
nanoclusters,<sup><xref ref-type="bibr" rid="ref14">14</xref></sup> and radioluminescent nanophosphors<sup><xref ref-type="bibr" rid="ref11">11</xref></sup> induces emissions similar to those observed
with traditional optical excitation. The use of X-rays allows for
probe excitation to occur at essentially any depth, eliminates the
background signal generated by tissue autofluorescence,<sup><xref ref-type="bibr" rid="ref15">15</xref></sup> and simplifies image reconstruction for optical
tomography.<sup><xref ref-type="bibr" rid="ref12">12</xref>,<xref ref-type="bibr" rid="ref16">16</xref></sup> Further modification of X-ray
excitable probes with targeting agents and antibodies will extend
the use of X-ray luminescence for applications in deep tissue molecular
and cellular imaging.</p><p>Here, we report on the development of
X-ray excitable RE probes with bright SWIR luminescence and demonstrate
their potential for deep tissue imaging applications. Previous reports
of X-ray luminescence have focused entirely on emissions in the visible
or NIR spectral region, neglecting the advantages afforded to SWIR
for deeper biological imaging. These advantages include reduced photon
absorption,<sup><xref ref-type="bibr" rid="ref1">1</xref></sup> scattering,<sup><xref ref-type="bibr" rid="ref17">17</xref></sup> and tissue autofluorescence<sup><xref ref-type="bibr" rid="ref4">4</xref></sup> that lead to deeper photon penetration in biological tissue<sup><xref ref-type="bibr" rid="ref5">5</xref>,<xref ref-type="bibr" rid="ref18">18</xref></sup> with high imaging fidelity.<sup><xref ref-type="bibr" rid="ref19">19</xref></sup> In this
report, we demonstrate a novel mechanism for inducing SWIR emissions
from various RE formulations using X-rays with ranging photon energies
and provide the first demonstration of X-ray induced SWIR emission
(X-IR) for biomedical imaging applications in nanoparticle tracking
and lymphatic mapping.</p><p>REs composed of NaYF<sub>4</sub> were
synthesized according to the well-established solvothermal decomposition
method<sup><xref ref-type="bibr" rid="ref20">20</xref></sup> and investigated for X-IR luminescence.
A core–shell structure was adopted for the nanoparticles by
first doping NaYF<sub>4</sub> with rare-earth elements and subsequently
surrounding the doped core with an undoped shell of NaYF<sub>4</sub>. The dopants chosen for this study were ytterbium (Yb) and erbium
(Er) with the trivalent erbium (Er<sup>3+</sup>) dopant acting as
the primary SWIR emitter. The NaYF<sub>4</sub> host was doped with
∼2% Er and 20% Yb, which has been previously shown to exhibit
the brightest visible<sup><xref ref-type="bibr" rid="ref21">21</xref></sup> and SWIR emissions.<sup><xref ref-type="bibr" rid="ref22">22</xref></sup> Both dopants were incorporated into the NaYF<sub>4</sub> host using their respective trifluoracetate (TFA) precursors
dissolved at ∼340 °C in the presence of an oleyamine surfactant.
The as-synthesized surfactant-capped REs displayed uniform morphology
(Figure <xref rid="fig1" ref-type="fig">1</xref>b) and were approximately 17.5 ±
2.3 nm in diameter (Figure <xref rid="fig1" ref-type="fig">1</xref>c) as measured
by transmission electron microscopy (TEM). The observed lattice fringes
were indicative of a predominately hexagonal (β) phase crystalline
structure corresponding to RE formulations shown to have the brightest
SWIR emission.<sup><xref ref-type="bibr" rid="ref23">23</xref></sup> To confirm the core–shell
structure of the REs, we synthesized “core-only”, doped
REs without the undoped NaYF<sub>4</sub> shell (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S1). We characterized the “core-only”
nanoparticles with TEM and found that the size distribution to be
significantly smaller from the core–shell REs (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S2), exhibiting
an average size of ∼8 nm likely due to the absence of the shell.
Qualitative analysis of RE atomic composition was obtained using energy-dispersive
X-ray spectroscopy (EDS) (Figure <xref rid="fig1" ref-type="fig">1</xref>d). Elemental
composition was estimated by comparing the relative peak intensities
of each element and matched the theoretical formulation (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S3).</p><p>To assess
the SWIR luminescence properties of REs, dried samples of REs were
packed into optically transparent cuvettes and irradiated with low-energy,
40 kVp X-rays. The characteristic SWIR emissions of the Er dopant
at 1525 nm were observed from the RE formulation using a SWIR detector
(NIRvana 640, Princeton Instruments) coupled to a spectrometer (Figure <xref rid="fig2" ref-type="fig">2</xref>a). The yttrium present in the host of the REs serves
as an effective X-ray absorber with a K-edge at 17.0 keV, which is
within the lower energy range for diagnostic X-rays. X-ray excitation
of the REs resulted in emissions that corresponded to those observed
following conventional NIR excitation (<xref rid="notes-4" ref-type="notes">Supporting
Information</xref> Figure S4). Energy transfer from the RE host lattice
to the luminescent dopants resulted in SWIR emission corresponding
to the characteristic Er<sup>3+</sup> peak at 1550 nm observed from
the <sup>4</sup>I<sub>13/2</sub> → <sup>4</sup>I<sub>15/2</sub> transition. Additional visible emissions characteristic of Er<sup>3+</sup> were detected at 540 and 650 nm after X-ray excitation (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S5), similar to
visible emissions observed after NIR excitation (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S6). While all visible emissions
are dominated by electric dipole transitions, the <sup>4</sup>I<sub>13/2</sub> → <sup>4</sup>I<sub>15/2</sub> transition resulting
in SWIR emissivity has been shown to contain both electric and magnetic
dipole contribution.<sup><xref ref-type="bibr" rid="ref24">24</xref></sup> Others have proposed
a possible mechanism describing the generation of X-ray luminescence
from REs through a stepwise process involving the formation of electron–hole
pairs (excitons), thermalization, excitation of the luminescent nanoparticle
centers (rare-earth dopants) through energy transfer from excitons,
relaxation of the excited luminescent center resulting in photon emission
and finally heat generation.<sup><xref ref-type="bibr" rid="ref25">25</xref></sup> This process
is highly dependent on various nanoparticle formulation parameters,
including the host material<sup><xref ref-type="bibr" rid="ref26">26</xref></sup> and its crystalline
phase<sup><xref ref-type="bibr" rid="ref25">25</xref></sup> as well as the concentration of
activator<sup><xref ref-type="bibr" rid="ref25">25</xref></sup> and fluoride ions.<sup><xref ref-type="bibr" rid="ref27">27</xref></sup> The optical stability of the REs in the presence
of high energy X-ray photons was evaluated under continuous irradiation.
REs were subjected to high-energy, 320 kVp X-rays and SWIR signal
intensity was monitored over time. The REs exhibited exceptional optical
stability, with less than a 3% change in emission intensity after
the delivery of a 50 Gy X-ray dose (Figure <xref rid="fig2" ref-type="fig">2</xref>b). These results confirm that REs are amenable toward repeated X-IR
imaging with minimal loss of signal.</p><fig id="fig2" position="float"><label>Figure 2</label><caption><p>X-IR spectrum of REs shows a distinct
SWIR emission peak centered around 1530 nm after X-ray irradiation
(a). REs retain SWIR emission intensity after extended exposure to
high energy (320 kVp) X-rays (b).</p></caption><graphic xlink:href="nl-2014-04123r_0003" id="gr2" position="float"></graphic></fig><p>In order to investigate the use of REs for biomedical X-IR
imaging applications, a cabinet irradiator unit was outfitted with
a lead-shielded SWIR detector positioned perpendicular to a light-tight
imaging space (Figure <xref rid="fig3" ref-type="fig">3</xref>a). The cabinet irradiator
allows for the delivery of superficial or orthovoltage X-rays at precise
photon energies and doses. Approximately 0.1 g of REs was pressed
into the 750 μm chambers of a hot spot resolution phantom (Micro
Deluxe Phantom, Data Spectrum Corporation). The imaging system was
capable of distinguishing the REs in the chambers and resolving X-IR
signal between two chambers filled with REs and spaced 1.50 mm apart
(Figure <xref rid="fig3" ref-type="fig">3</xref>b). To determine the temporal resolution
of the X-IR imaging system, SWIR emissions from 0.5 g of REs in a
SWIR transparent cuvette (UVette, Eppendorf) were captured under various
detector exposures following X-ray irradiation. The X-IR imaging system
was capable of resolving SWIR emissions with 1 ms exposure using 320
kVp (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S7)
and 80 kVp X-ray photons, and within 100 ms for low energy, 15 kVp
X-rays (Figure <xref rid="fig3" ref-type="fig">3</xref>c). All measurements were performed
with a tube current of 12.5 mA. Video-rate detection of SWIR signal
from REs opens the possibility for utilizing X-IR to conduct real-time
biomedical imaging, such as in vivo nanoparticle detection and tracking.</p><fig id="fig3" position="float"><label>Figure 3</label><caption><p>X-IR imaging
system consists of a highly sensitive SWIR detector and X-ray irradiator
cabinet enclosed within a light tight environment (a). X-IR was used
to image REs placed inside a resolution phantom with rods 0.75 mm
in diameter and 1.5 mm apart (b). Line profile across the phantom
(inset, yellow dashed line on image). Exposure sensitivity of the
X-IR imaging system was assessed by exciting REs under 80 kVp and
15 kVp X-rays (c). The X-IR detection sensitivity of REs was measured
as a function of X-ray accelerating voltage at a constant electric
current of 12.5 mA (d). Error bars represent pixel-to-pixel variation
within a region of interest and propagated over three samples.</p></caption><graphic xlink:href="nl-2014-04123r_0004" id="gr3" position="float"></graphic></fig><p>Next, the X-IR detection sensitivity
of REs in the presence of water was determined by dispersing the nanoparticles
in 2% agarose gels. Varying concentrations of REs (1.3 μM to
12.5 nM, corresponding to 10–0.1 mg mL<sup>–1</sup>)
were irradiated with X-rays and imaged using the SWIR detector. The
X-rays were conditioned with a 2 mm aluminum filter (HVL = ∼1
mm Cu) and all SWIR light between 800 and 1700 nm was collected by
the imaging system. REs could be detected at the lowest tested concentration
of 12.5 nM corresponding to 100 μg mL<sup>–1</sup> using
the X-IR imaging system (Figure <xref rid="fig3" ref-type="fig">3</xref>d). The molecular
weight of the REs were estimated from the average diameter of 18 nm
and the density of bulk NaYF<sub>4</sub> (4.21 g/cm<sup>3</sup>)<sup><xref ref-type="bibr" rid="ref4">4</xref>,<xref ref-type="bibr" rid="ref28">28</xref></sup> and found to be as ∼7 × 10<sup>6</sup> g/mol. For comparison,
we synthesized and evaluated the X-IR emission characteristics of
BaYF<sub>4</sub> nanoparticles doped with 20% Yb and 2% Er. Previous
studies have shown that, as with the NaYF<sub>4</sub> host, these
dopant concentrations generate the most efficient SWIR emission using
the BaYF<sub>4</sub> host.<sup><xref ref-type="bibr" rid="ref29">29</xref></sup> The same synthesis
procedure used to form the NaYF<sub>4</sub> nanoparticles was modified
with a barium precursor to fabricate the BaYF<sub>4</sub> nanoparticles.
Our previous work has shown BaYF<sub>4</sub> to be an effective host
for observing X-ray induced visible luminescence.<sup><xref ref-type="bibr" rid="ref11">11</xref></sup> BaYF<sub>4</sub> nanoparticles were found to exhibit similar
X-IR emission characteristics as the NaYF<sub>4</sub> REs (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S8) with comparable
optical stability (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S9). However, for similar X-ray photon energies, REs composed
of the NaYF<sub>4</sub> host were found to exhibit ∼25% greater
SWIR emission intensity at 1525 nm than ones synthesized with BaYF<sub>4</sub> on a weight percent basis (<xref rid="notes-4" ref-type="notes">Supporting
Information</xref> Figure S10). While both NaYF<sub>4</sub>- and BaYF<sub>4</sub>-based REs could be detected at 0.1 mg mL<sup>–1</sup>, the BaYF<sub>4</sub> nanoparticles required more energetic X-rays
for detection (160 kVp compared to 80 kVp) (<xref rid="notes-4" ref-type="notes">Supporting
Information</xref> Figure S10). It is important to note that accelerating
voltage also affects photon fluence and that for a given accelerating
tube voltage the X-ray beam contains a broad spectrum of photon energies.
Therefore, the X-IR emissions from both sets of REs display a strongly
linear dependence (<italic>R</italic><sup>2</sup> > 0.99) to absorbed
radiation dose, which suggests X-IR has the potential for quantitative
imaging applications. Subsequent studies will focus on optimizing
precise dopant schemes, as well as host composition, in order to systemically
evaluate the impact of these parameters on X-IR intensity.</p><p>The
translation of X-IR for preclinical imaging applications relies on
the development of contrast agents that exhibit favorable biological
properties while providing a high signal-to-noise ratio (SNR) for
distinguishing features of biomedical relevance.<sup><xref ref-type="bibr" rid="ref30">30</xref></sup> REs have been previously shown to be well-tolerated in
numerous in vivo studies<sup><xref ref-type="bibr" rid="ref31">31</xref>,<xref ref-type="bibr" rid="ref32">32</xref></sup> and there exists longer
term clinical translation potential for these materials with the FDA
approval of yttrium-based microparticles.<sup><xref ref-type="bibr" rid="ref33">33</xref></sup> However, as-synthesized REs are hydrophobic due to a surface surfactant
layer coating and quickly aggregate in aqueous solution. Therefore,
REs require further surface modification in order to enable aqueous
dispersion prior to biomedical use. Following synthesis and precipitation
of the REs with excess EtOH, the flocculated REs were isolated by
decanting the solvent and further purified by redispersion in toluene
and precipitation in EtOH. The isolated oleylamine coated REs were
rendered water-soluble with DSPE-2000-PEG by a ligand exchange procedure
performed under sonication in the presence of tetrahydrofuran (THF).
PEGylated REs were added dropwise into water and excess THF was allowed
to evaporate overnight. Any remaining aggregates were removed by a
0.22 μm filter. TEM imaging of PEG modified REs clearly showed
a 2.65 ± 0.65 nm amorphous “coating” surrounding
the crystalline REs that was notably absent in the unmodified particles
(Figure <xref rid="fig4" ref-type="fig">4</xref>a). This coating likely corresponds
to the layer of PEG added to the REs during ligand exchange. The water-soluble,
PEGylated REs exhibited a narrow hydrodynamic diameter centered at
100 nm (Figure <xref rid="fig4" ref-type="fig">4</xref>b) as determined by dynamic
light scattering (DLS), in comparison to as-synthesized REs that rapidly
aggregated in aqueous solution and displayed sizes above 1 μm
with high polydispersity (data not shown). The PEGylated REs were
stable in aqueous solution for up to a week postmodification with
minimal aggregation.</p><fig id="fig4" position="float"><label>Figure 4</label><caption><p>TEM of PEGylated REs reveals a uniform, amorphous coating
surrounding the nanoprobes (a). Most of the nanoprobe is imaged over
vacuum and the holey carbon support film is visible at the bottom
left edge of the image. DLS of PEGylated REs in PBS indicates monodispersed
particles around 100 nm in hydrodynamic diameter (b). PEGylated REs
were mixed with Matrigel and injected subcutaneously into regions
on the back flank of the mouse (c). X-IR imaging was performed using
320 kVp X-rays under 10 s exposure. Yellow circle indicates the sampled
region used for the background.</p></caption><graphic xlink:href="nl-2014-04123r_0005" id="gr4" position="float"></graphic></fig><p>Next, we evaluated the contrast capabilities of X-IR using
mock tumor inclusions implanted in nude mice. A mixture of PEG-modified
REs and Matrigel was subcutaneously injected into the back flanks
of the mice. Anesthetized mice were imaged over 30 s using our custom
X-IR imaging system operating under 320 kVp and 12.5 mA. SWIR emissions
from the 75 μM RE inclusion were clearly detectable from the
injection site with a complete absence of nonspecific autofluorescence
elsewhere on the animal (Figure <xref rid="fig4" ref-type="fig">4</xref>c). The signal-to-noise
ratio was calculated as the ratio of the X-IR signal amplitude to
the noise.<sup><xref ref-type="bibr" rid="ref34">34</xref></sup> A nearby region on the animal,
indicated by the yellow circle, was chosen to represent the typical
background signal observed during imaging. The SNR was then calculated
using the following equation<disp-formula id="eq1"><graphic xlink:href="nl-2014-04123r_m001" position="anchor"></graphic><label>1</label></disp-formula>Notably, there was an absence of observed
tissue autofluorescence during X-IR imaging, similar to what has been
previously reported during NIR excitation of REs.<sup><xref ref-type="bibr" rid="ref4">4</xref>,<xref ref-type="bibr" rid="ref10">10</xref></sup> Image
postprocessing revealed a ∼90 SNR between the X-IR signal from
the mock tumor inclusion to a nearby region on the mouse. A second
tumor inclusion with 10-fold more dilute REs (0.4 μM) was also
implanted into the back of the mouse and generated a SNR of ∼9.5.
For comparison, PEG-modified BaYF<sub>4</sub> nanoparticles were also
detectable after injection into the back of a mouse albeit at lower
SNRs (<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S11).
The magnitude of these ratios results from both the minimal endogenous
tissue autofluorescence of X-IR and exceptional SWIR signal production
of REs. Both the minimal tissue autofluorescence and deeper penetration
depth of X-ray photons provide significant improvements in SNR to
X-IR over traditional imaging techniques that rely on purely X-ray
or optical approaches. For example, our previous work has shown that
X-ray luminescence can improve the SNR for imaging by over 200% compared
to traditional X-ray fluoroscopy.<sup><xref ref-type="bibr" rid="ref35">35</xref></sup> Current
efforts are focused on evaluating the performance of X-IR relative
to traditional, NIR-induced SWIR imaging to better understand the
relationship of SNR on imaging conditions and between techniques.
The observed linear dependence of X-IR emissions on absorbed radiation
dose (Figure <xref rid="fig3" ref-type="fig">3</xref>d) as well as SNR on nanoparticle
concentration (Figure <xref rid="fig4" ref-type="fig">4</xref>c) suggests a similar
relationship between SNR and X-ray dose. While higher doses increase
the amount of SWIR photons from REs and may improve image quality,
the total amount of radiation delivered must be carefully monitored
when working with live animals.</p><p>We then assessed the ability
of X-IR to track and image the in vivo clearance of REs deep within
mice. The PEG-modified REs were intravenously injected into hairless
mice and imaged after 15 min using X-rays generated at 320 kVp and
12.5 mA. A standard digital camera was used to take the white light
image after the X-IR signal was captured. The biodistribution of REs
was visualized by their X-IR signature in organs mediating nanoparticle
clearance, such as the liver and spleen (Figure <xref rid="fig5" ref-type="fig">5</xref>a), similar to previous observations using NIR excitation.<sup><xref ref-type="bibr" rid="ref36">36</xref></sup> The fainter X-IR signal observed in the lungs
was likely due to nanoparticle accumulation or transient circulation
of the REs in the respiratory vascular network prior to sacrifice.
The X-IR signal from individual organs was confirmed after the organs
were excised. These results highlight the combined potential of using
a highly penetrating X-ray excitation source to detect an optical
signal with enhanced deep tissue resolution within a small animal
model. While the X-IR signal can be used to effectively monitor the
anatomical localization of REs, resolving that the finer details of
anatomical structure can be improved upon through several approaches.
It is likely breathing and organ motion artifacts are contributing
to a reduction in X-IR resolution similar to what has been observed
during X-ray CT imaging.<sup><xref ref-type="bibr" rid="ref37">37</xref></sup> Introducing
motion correction algorithms such as respiratory-gating<sup><xref ref-type="bibr" rid="ref38">38</xref>,<xref ref-type="bibr" rid="ref39">39</xref></sup> during image processing and using narrower X-ray excitation<sup><xref ref-type="bibr" rid="ref40">40</xref></sup> could be incorporated into a more optimized
X-IR imaging platform to improve spatial resolution further.</p><fig id="fig5" position="float"><label>Figure 5</label><caption><p>RE clearance
visualized in mice 15 min postinjection (p.i.) using X-IR imaging
at 320 kVp and 30 s exposure (a). White light images presented for
clarity. Organs were subsequently excised and imaged using X-IR to
confirm RE presence. Schematic of lymphatic mapping using X-IR of
PEGylated REs (b). PEGylated REs were injected into the footpad of
the mouse and imaged 45 min p.i. (c). Distinct focal luminescence
was visualized away from the injection site near the animal’s
axillary and brachial lymph nodes. After dissection, X-IR signal could
be traced to the local lymph nodes draining from the injection site
(axillary lymph node shown in the inset). In contrast, contralateral
lymph nodes did not show any notable X-IR signal.</p></caption><graphic xlink:href="nl-2014-04123r_0006" id="gr5" position="float"></graphic></fig><p>We further evaluated X-IR for imaging anatomical structures
with clinical importance. Sentinel lymph node mapping is a common
technique used to visualize lymph nodes near a primary tumor site
that are most likely to harbor metastases. Lymph node involvement
during cancer metastasis is important and commonly used for clinical
staging as well as assessing overall disease prognosis.<sup><xref ref-type="bibr" rid="ref41">41</xref></sup> Approximately 10 μL of 15 μM PEG-modified
REs were injected into the forepaw pad of anesthetized hairless mice.
These concentrations are comparable to intravenous doses of other
nanoparticle-based imaging formulations<sup><xref ref-type="bibr" rid="ref31">31</xref>,<xref ref-type="bibr" rid="ref42">42</xref>,<xref ref-type="bibr" rid="ref43">43</xref></sup> and similar to concentrations used by others for
X-ray luminescence imaging.<sup><xref ref-type="bibr" rid="ref44">44</xref></sup> After 45
min, the mouse was placed in the X-IR system and imaged using 320
kVp X-rays over 30 s. X-IR signal was observed to traverse into the
lower limb of the animal and accumulate in two distinct regions near
the draining lymph nodes (Figure <xref rid="fig5" ref-type="fig">5</xref>b), similar
to patterns of lymphatic drainage reported by others.<sup><xref ref-type="bibr" rid="ref45">45</xref>,<xref ref-type="bibr" rid="ref46">46</xref></sup> Upon dissection, both the brachial and axillary lymph nodes were
revealed to be the source of the observed X-IR emissions. Contralateral
lymph nodes were excised and compared by X-IR imaging. In contrast
to the nodes excised near the injection site, distant lymph nodes
did not display pronounced X-IR emissions. Notably, the lack of any
background from these distant lymph nodes highlights the exceptional
SNR of X-IR for sensitive imaging applications. The ability of X-IR
to resolve the finer details of lymphatic structure highlights the
potential of REs for imaging localized disease lesions. Combined with
molecular targeting strategies, the REs presented here could find
use for rapidly assessing tumor aggressiveness by screening lymph
node involvement during cancer metastasis with traditional X-ray diagnostic
techniques, such as computed tomography (CT) and mammography, or newer
imaging techniques such as X-ray tomosynthesis (Figure <xref rid="fig5" ref-type="fig">5</xref>c).<sup><xref ref-type="bibr" rid="ref47">47</xref></sup></p><p>While NIR excitation
of REs may offer advantages over X-IR for certain imaging applications,
notably intraoperative or subsurface imaging, X-IR may be useful in
clinical practices that involve X-rays or X-ray imaging. For example,
X-IR may be useful for classifying disease status during the delivery
of radiation therapy, enabling the identification of tumor margins
by surgeons or quantification of delivery dose by radiation oncologists.
In addition, raster scanning a narrow X-ray pencil beam through tissue
can be used to generate optical scatter-free images of RE distribution
with precise localization of the emitting nanoprobes source. Monte
Carlo simulations were run to highlight the benefits of scatter-free
pencil beam X-ray excitation compared to traditional NIR excitation
(<xref rid="notes-4" ref-type="notes">Supporting Information</xref> Figure S12).</p><p>As previously mentioned, the total radiation dose delivered must
be monitored when working with live animals in any X-ray or nuclear
imaging modality. Current microCT systems generally deliver a dose
on the order of 10 cGy to rodents,<sup><xref ref-type="bibr" rid="ref48">48</xref></sup> while
small animal SPECT and PET systems may deliver up to almost 100 cGy
of whole body dose per experiment.<sup><xref ref-type="bibr" rid="ref49">49</xref></sup> On
the basis of our current setup, our delivered dose would be on the
order of 50–250 cGy depending on the exposure and accelerating
voltage used. While this still is below the LD50/30 for radiation
dose in mice (estimated at ∼7 Gy),<sup><xref ref-type="bibr" rid="ref50">50</xref>,<xref ref-type="bibr" rid="ref51">51</xref></sup> high X-ray dose can affect the quantitative accuracy of longitudinal
studies due to unwanted radiation-induced side effects.<sup><xref ref-type="bibr" rid="ref52">52</xref></sup> We anticipate that further improvements to both
our imaging setup and formulation will reduce the doses delivered
in this proof-of-concept study significantly. For example, our previous
work has shown a subpicomolar detection sensitivity of nanoparticles
using selective X-ray excitation at doses below 1 cGy,<sup><xref ref-type="bibr" rid="ref53">53</xref></sup> while others have noted significant improvements
in X-ray luminescence intensity based on changes in nanoparticle composition.<sup><xref ref-type="bibr" rid="ref25">25</xref></sup></p><p>Our work presents the first demonstration
of SWIR tissue imaging using diagnostic and therapeutic X-rays. By
capitalizing on the exceptional tissue penetrating properties of X-rays,
our work builds on recent reports utilizing visible X-ray luminescence
for monitoring nanoparticle organ accumulation<sup><xref ref-type="bibr" rid="ref54">54</xref>,<xref ref-type="bibr" rid="ref55">55</xref></sup> and advances nonvisible X-ray luminescence for high resolution,
deep tissue anatomical imaging of nanoparticle biodistribution using
SWIR light. Crucially, we are the first to show the capabilities of
X-IR imaging for mapping lymphatic drainage of biologically modified
nanoparticles at resolutions and SNR sufficient to identify individual
nodes. Unlike other imaging approaches that combine imaging techniques
such as nuclear/CT, nuclear/magnetic resonance, or CT/fluorescence
molecular tomography, X-IR imaging does not rely on two independent
imaging devices but instead combines the advantages of both X-ray
and optical imaging synergistically to produce visual data that would
otherwise not have been possible using either modality alone.</p><p>The implications of this proposed imaging technique will provide
a new paradigm for preclinical and future clinical applications. For
example, X-IR could be used to enrich CT imaging with spatially registered
molecular information. By conjugating REs with targeted biomolecules,
X-IR can be used to bridge gross anatomical X-ray imaging with the
optical detection of targeted molecular biomarkers specific to disease
states. Furthermore, the REs presented in this study were fabricated
with erbium doping; however, other dopant schemes including holmium–ytterbium,
thulium–ytterbium, and praseodymium–ytterbium can be
used for tuning the peak emission wavelengths of the REs. Developing
a library of such formulations opens the possibility for extending
X-IR toward multispectral imaging applications and refining X-IR for
simultaneously monitoring the interplay between multiple biological
processes in vivo.</p></body><back><notes id="notes-4" notes-type="si"><title>Supporting Information Available</title><p>Supplemental methods, nanoparticle characterization,
BaYF<sub>4</sub>:Er,Yb optical and X-IR properties. This material
is available free of charge via the Internet at <uri xlink:href="http://pubs.acs.org">http://pubs.acs.org</uri>.</p></notes><sec sec-type="supplementary-material"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="sifile1"><media xlink:href="nl504123r_si_001.pdf"><caption><p>nl504123r_si_001.pdf</p></caption></media></supplementary-material></sec><notes id="notes-1"><title>Author Contributions</title><p>The manuscript was written through
contributions of all authors. All authors have given approval to the
final version of the manuscript.</p></notes><notes id="notes-3" notes-type="funding-statement"><p>The authors are grateful for funding
support offered by the NIBIB (1R01 EB016777), NCI (1R01 CA133474),
and the U.S. Department of Defense, Breast Cancer Research Program
award W81XWH-11-1-0087.</p></notes><notes id="notes-2" notes-type="conflict-of-interest"><p>The authors declare no competing
financial interest.</p></notes><glossary id="dl1"><def-list><title>Abbreviations</title><def-item><term>RE</term><def><p>rare-earth doped nanoprobes</p></def></def-item><def-item><term>SWIR and NIR-II</term><def><p>shortwave
infrared</p></def></def-item><def-item><term>X-IR</term><def><p>X-ray
induced SWIR luminescence (X-IR)</p></def></def-item><def-item><term>QD</term><def><p>quantum dots</p></def></def-item><def-item><term>NIR</term><def><p>near-infrared</p></def></def-item><def-item><term>TEM</term><def><p>transmission electron microscopy</p></def></def-item><def-item><term>EDS</term><def><p>energy dispersive X-ray spectroscopy</p></def></def-item><def-item><term>CT</term><def><p>computed tomography</p></def></def-item><def-item><term>HVL</term><def><p>half value layer</p></def></def-item><def-item><term>p.i</term><def><p>postinjection</p></def></def-item><def-item><term>MR</term><def><p>magnetic resonance</p></def></def-item><def-item><term>FMT</term><def><p>fluorescence molecular
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