Anticancer Ruthenium(III) Complexes and Ru(III)-Containing Nanoformulations: An Update on the Mechanism of Action and Biological Activity
Identifieur interne : 000A94 ( Pmc/Curation ); précédent : 000A93; suivant : 000A95Anticancer Ruthenium(III) Complexes and Ru(III)-Containing Nanoformulations: An Update on the Mechanism of Action and Biological Activity
Auteurs : Claudia Riccardi ; Domenica Musumeci ; Marco Trifuoggi ; Carlo Irace ; Luigi Paduano ; Daniela MontesarchioSource :
- Pharmaceuticals [ 1424-8247 ] ; 2019.
Abstract
The great advances in the studies on metal complexes for the treatment of different cancer forms, starting from the pioneering works on platinum derivatives, have fostered an increasingly growing interest in their properties and biomedical applications. Among the various metal-containing drugs investigated thus far, ruthenium(III) complexes have emerged for their selective cytotoxic activity in vitro and promising anticancer properties in vivo, also leading to a few candidates in advanced clinical trials. Aiming at addressing the solubility, stability and cellular uptake issues of low molecular weight Ru(III)-based compounds, some research groups have proposed the development of suitable drug delivery systems (e.g., taking advantage of nanoparticles, liposomes, etc.) able to enhance their activity compared to the naked drugs. This review highlights the unique role of Ru(III) complexes in the current panorama of anticancer agents, with particular emphasis on Ru-containing nanoformulations based on the incorporation of the Ru(III) complexes into suitable nanocarriers in order to enhance their bioavailability and pharmacokinetic properties. Preclinical evaluation of these nanoaggregates is discussed with a special focus on the investigation of their mechanism of action at a molecular level, highlighting their pharmacological potential in tumour disease models and value for biomedical applications.
Url:
DOI: 10.3390/ph12040146
PubMed: 31561546
PubMed Central: 6958509
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Montesano 49, I-80131 Naples, Italy;<email>carlo.irace@unina.it</email></nlm:aff></affiliation></author><author><name sortKey="Paduano, Luigi" sort="Paduano, Luigi" uniqKey="Paduano L" first="Luigi" last="Paduano">Luigi Paduano</name><affiliation><nlm:aff id="af1-pharmaceuticals-12-00146">Department of Chemical Sciences, University of Naples Federico II, Via Cintia 21, I-80126 Naples, Italy;<email>claudia.riccardi@unina.it</email> (C.R.);<email>domenica.musumeci@unina.it</email> (D.M.);<email>marco.trifuoggi@unina.it</email> (M.T.);<email>luigi.paduano@unina.it</email> (L.P.)</nlm:aff></affiliation></author><author><name sortKey="Montesarchio, Daniela" sort="Montesarchio, Daniela" uniqKey="Montesarchio D" first="Daniela" last="Montesarchio">Daniela Montesarchio</name><affiliation><nlm:aff id="af1-pharmaceuticals-12-00146">Department of Chemical Sciences, University of Naples Federico II, Via Cintia 21, I-80126 Naples, Italy;<email>claudia.riccardi@unina.it</email> (C.R.);<email>domenica.musumeci@unina.it</email> (D.M.);<email>marco.trifuoggi@unina.it</email> (M.T.);<email>luigi.paduano@unina.it</email> (L.P.)</nlm:aff></affiliation></author></analytic><series><title level="j">Pharmaceuticals</title><idno type="eISSN">1424-8247</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The great advances in the studies on metal complexes for the treatment of different cancer forms, starting from the pioneering works on platinum derivatives, have fostered an increasingly growing interest in their properties and biomedical applications. Among the various metal-containing drugs investigated thus far, ruthenium(III) complexes have emerged for their selective cytotoxic activity in vitro and promising anticancer properties in vivo, also leading to a few candidates in advanced clinical trials. Aiming at addressing the solubility, stability and cellular uptake issues of low molecular weight Ru(III)-based compounds, some research groups have proposed the development of suitable drug delivery systems (e.g., taking advantage of nanoparticles, liposomes, etc.) able to enhance their activity compared to the naked drugs. This review highlights the unique role of Ru(III) complexes in the current panorama of anticancer agents, with particular emphasis on Ru-containing nanoformulations based on the incorporation of the Ru(III) complexes into suitable nanocarriers in order to enhance their bioavailability and pharmacokinetic properties. Preclinical evaluation of these nanoaggregates is discussed with a special focus on the investigation of their mechanism of action at a molecular level, highlighting their pharmacological potential in tumour disease models and value for biomedical applications.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Rosenberg, B" uniqKey="Rosenberg B">B. Rosenberg</name></author><author><name sortKey="Vancamp, L" uniqKey="Vancamp L">L. Vancamp</name></author><author><name sortKey="Krigas, T" uniqKey="Krigas T">T. Krigas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rosenberg, B" uniqKey="Rosenberg B">B. Rosenberg</name></author><author><name sortKey="Van Camp, L" uniqKey="Van Camp L">L. van Camp</name></author><author><name sortKey="Trosko, J E" uniqKey="Trosko J">J.E. Trosko</name></author><author><name sortKey="Mansour, V H" uniqKey="Mansour V">V.H. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Pharmaceuticals (Basel)</journal-id><journal-id journal-id-type="iso-abbrev">Pharmaceuticals (Basel)</journal-id><journal-id journal-id-type="publisher-id">pharmaceuticals</journal-id><journal-title-group><journal-title>Pharmaceuticals</journal-title></journal-title-group><issn pub-type="epub">1424-8247</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31561546</article-id><article-id pub-id-type="pmc">6958509</article-id><article-id pub-id-type="doi">10.3390/ph12040146</article-id><article-id pub-id-type="publisher-id">pharmaceuticals-12-00146</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Anticancer Ruthenium(III) Complexes and Ru(III)-Containing Nanoformulations: An Update on the Mechanism of Action and Biological Activity</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-7182-0757</contrib-id><name><surname>Riccardi</surname><given-names>Claudia</given-names></name><xref ref-type="aff" rid="af1-pharmaceuticals-12-00146">1</xref></contrib><contrib contrib-type="author"><name><surname>Musumeci</surname><given-names>Domenica</given-names></name><xref ref-type="aff" rid="af1-pharmaceuticals-12-00146">1</xref></contrib><contrib contrib-type="author"><name><surname>Trifuoggi</surname><given-names>Marco</given-names></name><xref ref-type="aff" rid="af1-pharmaceuticals-12-00146">1</xref></contrib><contrib contrib-type="author"><name><surname>Irace</surname><given-names>Carlo</given-names></name><xref ref-type="aff" rid="af2-pharmaceuticals-12-00146">2</xref></contrib><contrib contrib-type="author"><name><surname>Paduano</surname><given-names>Luigi</given-names></name><xref ref-type="aff" rid="af1-pharmaceuticals-12-00146">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-6295-6911</contrib-id><name><surname>Montesarchio</surname><given-names>Daniela</given-names></name><xref ref-type="aff" rid="af1-pharmaceuticals-12-00146">1</xref><xref rid="c1-pharmaceuticals-12-00146" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-pharmaceuticals-12-00146"><label>1</label>Department of Chemical Sciences, University of Naples Federico II, Via Cintia 21, I-80126 Naples, Italy;<email>claudia.riccardi@unina.it</email> (C.R.);<email>domenica.musumeci@unina.it</email> (D.M.);<email>marco.trifuoggi@unina.it</email> (M.T.);<email>luigi.paduano@unina.it</email> (L.P.)</aff><aff id="af2-pharmaceuticals-12-00146"><label>2</label>Department of Pharmacy, University of Naples Federico II, Via D. Montesano 49, I-80131 Naples, Italy;<email>carlo.irace@unina.it</email></aff><author-notes><corresp id="c1-pharmaceuticals-12-00146"><label>*</label>Correspondence: <email>daniela.montesarchio@unina.it</email></corresp></author-notes><pub-date pub-type="epub"><day>26</day><month>9</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>12</month><year>2019</year></pub-date><volume>12</volume><issue>4</issue><elocation-id>146</elocation-id><history><date date-type="received"><day>31</day><month>8</month><year>2019</year></date><date date-type="accepted"><day>23</day><month>9</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>The great advances in the studies on metal complexes for the treatment of different cancer forms, starting from the pioneering works on platinum derivatives, have fostered an increasingly growing interest in their properties and biomedical applications. Among the various metal-containing drugs investigated thus far, ruthenium(III) complexes have emerged for their selective cytotoxic activity in vitro and promising anticancer properties in vivo, also leading to a few candidates in advanced clinical trials. Aiming at addressing the solubility, stability and cellular uptake issues of low molecular weight Ru(III)-based compounds, some research groups have proposed the development of suitable drug delivery systems (e.g., taking advantage of nanoparticles, liposomes, etc.) able to enhance their activity compared to the naked drugs. This review highlights the unique role of Ru(III) complexes in the current panorama of anticancer agents, with particular emphasis on Ru-containing nanoformulations based on the incorporation of the Ru(III) complexes into suitable nanocarriers in order to enhance their bioavailability and pharmacokinetic properties. Preclinical evaluation of these nanoaggregates is discussed with a special focus on the investigation of their mechanism of action at a molecular level, highlighting their pharmacological potential in tumour disease models and value for biomedical applications.</p></abstract><kwd-group><kwd>Ruthenium(III) complexes</kwd><kwd>nanocarriers</kwd><kwd>nanoaggregates</kwd><kwd>drug delivery</kwd><kwd>anticancer therapy</kwd><kwd>preclinical evaluation</kwd></kwd-group></article-meta></front><floats-group><fig id="pharmaceuticals-12-00146-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Chemical structures of NAMI-A, KP1019, NKP-1339 and AziRu. Here, ruthenium ions are indicated in red, the counterions in green, while the N- and S-donor ligands in dark and light blue, respectively.</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g001"></graphic></fig><fig id="pharmaceuticals-12-00146-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Chemical structures of the proposed nucleolipid and aminoacyl lipid-based Ru(III)-complexes. In the figures, ruthenium ions are indicated in red, the central scaffolds in green, while the hydrophilic and lipophilic chains in dark and light blue, respectively. In the HoThyDansRu molecular structure, the fluorescent dansyl group is highlighted in yellow (Bn = benzyl group).</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g002"></graphic></fig><fig id="pharmaceuticals-12-00146-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>KP1019 incorporation into polylactic acid nanoparticles (PLA NPs): (<bold>a</bold>) chemical structures of polylactic acid and of the surfactant used in the formulation (poloxamer Pluronic F-68 and polysorbate Tween 80); (<bold>b</bold>) nanoparticle appearance after different temperature and period storage: TWNP_3 (5 d, 4 °C), TWNP_2 (24 h, 4 °C), TWNP_4 (24 h, 25 °C), TWNP_1 (2 h, 25 °C), blank TWNP, from left to right; (<bold>c</bold>) IC<sub>50</sub> values (µM) of the different KP1019 nanoformulations prepared in comparison with naked KP1019. Blank TWNP_1 (1 month, 4 °C), Blank TWNP_2 (2 h, 25 °C); IC<sub>50</sub> values are reported as mean ± SEM. (<bold>d</bold>) dose-response curves of colon carcinoma SW480 and the hepatoma Hep3B cancer cell lines with the indicated drugs as determined by MTT assay after 72 h treatment. Figures were adapted from [<xref rid="B111-pharmaceuticals-12-00146" ref-type="bibr">111</xref>] published by The Royal Society of Chemistry.</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g003"></graphic></fig><fig id="pharmaceuticals-12-00146-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>NAMI-A conjugation to polymeric micelles: (<bold>a</bold>) chemical structure of the amphiphilic block copolymer P(NAMI-A)-PPEGMEA and schematic representation of its micellization in water; (<bold>b</bold>) cytotoxicity and IC<sub>50</sub> values (µM, expressed in terms of ruthenium concentration) of NAMI-A and P(NAMI-A)-PPEGMEA against ovarian A2780 and Ovcar-3 and pancreatic AsPC-1 cancer cell lines. IC<sub>50</sub> values are reported as mean ± SEM. Figures were adapted with permission from [<xref rid="B115-pharmaceuticals-12-00146" ref-type="bibr">115</xref>] Copyright 2014 from American Chemical Society.</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g004"></graphic></fig><fig id="pharmaceuticals-12-00146-f005" orientation="portrait" position="float"><label>Figure 5</label><caption><p>Pyridine-containing Ru(III) complexes inserted in liposome systems: (<bold>a</bold>) chemical structure of the proposed RuPy and RuPyTry compounds; (<bold>b</bold>) schematic representation of liposomal nanoaggregates containing the pyridine-based Ru(III) complexes; (<bold>c</bold>) dose-response histograms reporting the cytotoxic effects observed for the naked Ru(III) compounds and their liposomal formulations in PC-3 cancer cells after 48 h treatment. Figures are adapted from [<xref rid="B116-pharmaceuticals-12-00146" ref-type="bibr">116</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g005"></graphic></fig><fig id="pharmaceuticals-12-00146-f006" orientation="portrait" position="float"><label>Figure 6</label><caption><p>(<bold>a</bold>) Chemical structures of mononuclear and dinuclear Ru(III)-dithiocarbamato complexes and of the investigated dithiocarbamato ligands: pyrrolidyl dithiocarbamate (PDT) and carbazolyl dithiocarbamate (CDT); (<bold>b</bold>) schematic representation of the Pluronic<sup>®</sup> F127 block copolymer and micelle formation with Ru(III) complex internalization; (<bold>c</bold>) IC<sub>50</sub> values (μM) evaluated after 72 h treatment with free Ru(III)-dithiocarbamato complexes and their micelles formulations (indicated as PL{compound}). IC<sub>50</sub> values are reported as mean ± SEM. Figures are adapted from [<xref rid="B117-pharmaceuticals-12-00146" ref-type="bibr">117</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g006"></graphic></fig><fig id="pharmaceuticals-12-00146-f007" orientation="portrait" position="float"><label>Figure 7</label><caption><p>Schematic representation of liposomal POPC- or DOTAP-based nanoaggregates containing nucleolipid- or aminoacyl lipid-based Ru(III) complexes.</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g007"></graphic></fig><fig id="pharmaceuticals-12-00146-f008" orientation="portrait" position="float"><label>Figure 8</label><caption><p>Human MCF-7 breast adenocarcinoma cells incubated with 100 µM HoThyDansRu/DOTAP liposome formulations and followed at different times: (<bold>a</bold>) fluorescent photomicrographs of cell monolayers showing the cellular localization of the fluorescent HoThyDansRu/DOTAP liposomes; (<bold>b</bold>) confocal microscopy bioimaging showing the cellular uptake of the fluorescent HoThyDansRu/DOTAP nanosystem. DAPI was used as a nuclear stain (shown in blue). Dansyl-dependent fluorescence (Dans) of HoThyDansRu/DOTAP liposomes is shown in red (<bold>a</bold>) or as green dots (<bold>b</bold>). E-cadherine-associated fluorescence (CAD), defining cell shape, is shown in red (<bold>b</bold>). In merged images (Merge), the two fluorescent emission patterns are overlapped. Insets in panel <bold>a</bold> represent higher magnifications of merged images showing cellular location of fluorescent dansylated ruthenium complexes. Figures were adapted with permission from [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>] Copyright (2013) American Chemical Society (<bold>a</bold>) and from [<xref rid="B100-pharmaceuticals-12-00146" ref-type="bibr">100</xref>] (<bold>b</bold>).</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g008"></graphic></fig><fig id="pharmaceuticals-12-00146-f009" orientation="portrait" position="float"><label>Figure 9</label><caption><p>Representative photomicrographs by phase-contrast light microscopy showing the cellular morphological changes and cytotoxic effects on cellular monolayers: untreated (left column in panels <bold>a</bold> and <bold>b</bold>) or treated for 48 h with ToThyRu/POPC (<bold>a</bold>) or ToThyCholRu/DOTAP (<bold>b</bold>) formulations. For ToThyRu/POPC nanosystems, MCF-7, WiDr and C6 cancer cell lines were examined (<bold>a</bold>); in turn, for ToThyCholRu/DOTAP nanocarriers, MCF-7, WiDr and HeLa cancer cell lines were analysed (<bold>b</bold>). Insets in (a) represent higher magnifications of injured cells following incubations with ToThyRu/POPC liposomes. (<bold>c</bold>) MCF-7 and MDA-MB-231 breast cancer cells treated for 48 and 72 h with ruthenium IC<sub>50</sub> concentrations of DoHuRu-containing liposomes. The inset in (c) represents higher magnifications at 0 (left panel) and 48 h (right panel) DoHuRu/DOTAP treated MCF-7 cells, showing the formation of autophagic vacuoles detectable in cell cytoplasm. Figures are adapted from [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>] (<bold>a</bold>), [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>] (<bold>b</bold>) and [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>] (<bold>c</bold>).</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g009"></graphic></fig><fig id="pharmaceuticals-12-00146-f010" orientation="portrait" position="float"><label>Figure 10</label><caption><p>Induction of apoptosis in MCF-7 (<bold>a</bold>) and MDA-MB-231(<bold>b</bold>) breast cancer cells, evaluated by FACS analysis (right on each panel), after cell labelling with propidium iodide (PI) and FITC-Annexin V. Cells were both unlabelled and untreated (CTR −), labelled and not treated (CTR +), treated with IC<sub>50</sub> doses of DoHuRu-incorporating POPC or DOTAP liposomes for 48 and 72 h, as indicated. The quantitative analysis of viable, non-viable (necrotic), early and late apoptotic cells after drug exposure is represented (bar graphs on the right of each panel). Viable cells are negative for both PI and FITC-Annexin V binding; non-viable, necrotic cells are negative for FITC-Annexin V binding and positive for PI uptake; cells in early apoptosis are FITC-Annexin V positive and PI negative; cells in late apoptosis are positive for both FITC-Annexin V binding and PI uptake. Figures were adapted from [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g010"></graphic></fig><fig id="pharmaceuticals-12-00146-f011" orientation="portrait" position="float"><label>Figure 11</label><caption><p>1.5% agarose gels representing the DNA fragmentation assay on MCF-7, WiDr and HeLa cells, treated or not (Ctrl) for 48 h with IC<sub>50</sub> doses of ToThyCholRu–DOTAP liposomes (indicated as Ru) (<bold>a</bold>) and MCF-7 and MDA-MB-321 cells treated or not (C) with IC<sub>50</sub> concentrations of DoHuRu/POPC (Ru<sup>POPC</sup>) and DoHuRu/DOTAP (Ru<sup>DOTAP</sup>) for 48 h (<bold>b</bold>). In both experiments, the selected cell lines were also treated with IC<sub>50</sub> conc. of cisplatin (cDDP) used as a control. Lane M corresponds to the molecular weight markers. Figures are adapted from [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>] (<bold>a</bold>) and [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>] (<bold>b</bold>).</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g011"></graphic></fig><fig id="pharmaceuticals-12-00146-f012" orientation="portrait" position="float"><label>Figure 12</label><caption><p>Schematic representation of the intrinsic (or mitochondrial) and the extrinsic (or death receptor) apoptotic pathways.</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g012"></graphic></fig><fig id="pharmaceuticals-12-00146-f013" orientation="portrait" position="float"><label>Figure 13</label><caption><p>Western blot analysis showing the effects of IC<sub>50</sub> doses of DoHuRu/POPC and DoHuRu/DOTAP following 48 and 72 h of incubation in MCF-7 (<bold>a</bold>) and MDA-MB-231 (<bold>b</bold>) cells on caspases-3, -8 and -9 expression and activation, and on Bax and BCL-2 expression. Bands resulting after chemoluminescence from treated cells were extracted, quantified by densitometric analysis and then plotted (graphs on the right of each panel): solid and dotted lines for Bax and BCL-2 expression proteins, respectively, and bar graphs (caspases-3, -8 and -9) reported as percentage of control in relation to the used Ru-containing nanoaggregates. Figures are adapted from [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g013"></graphic></fig><fig id="pharmaceuticals-12-00146-f014" orientation="portrait" position="float"><label>Figure 14</label><caption><p>Quantitative flow cytometric analysis of autophagosomes formation (MDC incorporation) in MCF-7 (<bold>a</bold>) and MDA-MD-231(<bold>b</bold>) breast cancer cells for the autophagy activation evaluation: unlabelled and untreated (CTR −), labelled and untreated (CTR +), treated with IC<sub>50</sub> concentrations of DoHuRu/POPC or with DoHuRu/DOTAP formulations for 48 and 72 h, as indicated. In the bar graphs, calculated main fluorescence intensities (MFIs) values are expressed as percentage of control cells. Figures are adapted from [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g014"></graphic></fig><fig id="pharmaceuticals-12-00146-f015" orientation="portrait" position="float"><label>Figure 15</label><caption><p>Western blot analysis showing the effects of IC<sub>50</sub> doses of HoThyRu/DOTAP liposomes following 48 and 72 h of incubation in MCF-7 (<bold>a</bold>) and MDA-MB-231 cells (<bold>b</bold>) on LC3-I, LC3-II, Bax, BCL-2, and Becli-1 expression (Ctrl, untreated cells at the time zero). Bands resulting from MCF-7 and MDA-MB-231 cells were extracted, quantified by densitometric analysis and then plotted in bar graphs (right of each panel) as percentage of controls. Figures are adapted from [<xref rid="B100-pharmaceuticals-12-00146" ref-type="bibr">100</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g015"></graphic></fig><fig id="pharmaceuticals-12-00146-f016" orientation="portrait" position="float"><label>Figure 16</label><caption><p>In vivo anticancer effects of HoThyRu/DOTAP nanosystems: tumour photographs after the collection (<bold>a</bold>); tumour weight (<bold>b</bold>) and tumour size (<bold>c</bold>) evaluation; mice survival (<bold>d</bold>) and body weight (<bold>e</bold>) determination (PBS control group, Ru treated group). Figures are adapted from [<xref rid="B100-pharmaceuticals-12-00146" ref-type="bibr">100</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g016"></graphic></fig><fig id="pharmaceuticals-12-00146-f017" orientation="portrait" position="float"><label>Figure 17</label><caption><p>Schematic representation of niosome formulations based on a cationic aminolipid and the polysorbate 80, also containing the nucleolipid-based Ru(III) complex HoThyRu along with AS1411. On the right, the concentration/effects bar graphs obtained after in vitro treatment on HeLa cancer cells were also reported as representative examples. Figures were adapted from [<xref rid="B109-pharmaceuticals-12-00146" ref-type="bibr">109</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g017"></graphic></fig><fig id="pharmaceuticals-12-00146-f018" orientation="portrait" position="float"><label>Figure 18</label><caption><p>18LPC-ToThyCholRu/SPIONs: schematic representation of NPs systems with the inner membrane layer based on oleylamine/oleic acid and the outer membrane layer composed of 18-LPC loaded with the Ru(III)-complex ToThyCholRu (<bold>a</bold>); IC<sub>50</sub> values (μM)—reported as mean ± SEM—relative to the effective ruthenium concentration carried by 18LPC-ToThyCholRu/SPIONs in the indicated cell lines following 48 h incubation (<bold>b</bold>); representative photomicrographs by phase-contrast light microscopy (<bold>c</bold>) of MCF-7 cell lines untreated (control cells, left) or treated for 48 h with the indicated iron concentration of 18LPC/SPIONs (top line) and of 18LPC-ToThyCholRu/SPIONs (bottom line); MRI measurements (<bold>d</bold>): transverse relaxation rate (R<sub>2</sub> = 1/T<sub>2</sub>, s<sup>−1</sup>) measured after bolus injection in the tail vein of 18LPC/SPIONs in 0.9% NaCl solution (top) with inset representing the ROI, selected in the coronal plane covering the liver; T<sub>2</sub>-weighted image of a coronal view of the animal (Wistar rat) before injection of the 18LPC/SPIONs (bottom, left); representative T<sub>2</sub>-mapping MRI image of a coronal view after injection (t = 3 min) of the 18LPC/SPIONs (bottom, right). Figures are adapted from [<xref rid="B108-pharmaceuticals-12-00146" ref-type="bibr">108</xref>].</p></caption><graphic xlink:href="pharmaceuticals-12-00146-g018"></graphic></fig><table-wrap id="pharmaceuticals-12-00146-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">pharmaceuticals-12-00146-t001_Table 1</object-id><label>Table 1</label><caption><p>IC<sub>50</sub> values (µM) relative to AziRu and to the effective ruthenium concentration inserted in the Ru(III)-incorporating POPC- and DOTAP-based liposomes in the indicated cell lines following 48 or 72 h of incubation in vitro. IC<sub>50</sub> values are reported as mean ± SEM.</p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="7" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">IC<sub>50</sub> (μM)</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MCF-7</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">WiDr</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C6</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HeLa</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">L6</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HaCaT</th></tr></thead><tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NAMI-A [<xref rid="B78-pharmaceuticals-12-00146" ref-type="bibr">78</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">620 ± 30</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">626 ± 45</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AziRu [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>,<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">305 ± 16 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">441 ± 20 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">318 ± 12 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">382 ± 19 [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">> 500 [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">> 500 [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td></tr><tr><td colspan="7" align="center" valign="middle" style="border-bottom:solid thin" rowspan="1">POPC-based formulations</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ToThyRu/POPC [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>,<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">27.8 ± 0.1 [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">75 ± 4 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">36 ± 8 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HoThyRu/POPC [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">7 ± 4</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">40 ± 5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">81 ± 7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DoHuRu/POPC [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>,<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">18.9 ± 0.1 [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">99 ± 5 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24 ± 5 [<xref rid="B77-pharmaceuticals-12-00146" ref-type="bibr">77</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ToThyCholRu/POPC [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>,<xref rid="B105-pharmaceuticals-12-00146" ref-type="bibr">105</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">70 ± 12 [<xref rid="B105-pharmaceuticals-12-00146" ref-type="bibr">105</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">165 ± 10 [<xref rid="B105-pharmaceuticals-12-00146" ref-type="bibr">105</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">>500 [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">>500 [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HoUrRu/POPC [<xref rid="B107-pharmaceuticals-12-00146" ref-type="bibr">107</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">14 ± 7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">20 ± 8</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td colspan="7" align="center" valign="middle" style="border-bottom:solid thin" rowspan="1">DOTAP-based formulations</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ToThyRu/DOTAP [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>,<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">10.1 ± 0.1 [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">50 ± 11 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">54 ± 8 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HoThyRu/DOTAP [<xref rid="B100-pharmaceuticals-12-00146" ref-type="bibr">100</xref>,<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">13 ± 4 [<xref rid="B100-pharmaceuticals-12-00146" ref-type="bibr">100</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">65 ± 8 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">43 ± 11 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DoHuRu/DOTAP [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>,<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">10.3 ± 0.2 [<xref rid="B134-pharmaceuticals-12-00146" ref-type="bibr">134</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">41 ± 10 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">34 ± 9 [<xref rid="B106-pharmaceuticals-12-00146" ref-type="bibr">106</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ToThyCholRu/DOTAP [<xref rid="B79-pharmaceuticals-12-00146" ref-type="bibr">79</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">13 ± 2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">23 ± 8</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">34 ± 4</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">187 ± 1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">377 ± 3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HoUrRu/DOTAP [<xref rid="B107-pharmaceuticals-12-00146" ref-type="bibr">107</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">8 ± 5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">12 ± 5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">I/DOTAP [<xref rid="B110-pharmaceuticals-12-00146" ref-type="bibr">110</xref>]</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">31.2 ± 2.7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">35.4 ± 2.7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">45.6 ± 3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">>150</td></tr></tbody></table></table-wrap><table-wrap id="pharmaceuticals-12-00146-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">pharmaceuticals-12-00146-t001_Table 2</object-id><label>Table 1</label><caption><p>Host range and plaque morphology of the 19 phages examined in this paper. Phages were isolated from various environments: natural springs, industrial waste water and chicken meat. The infectivity of the phages was calculated based on the host range (<xref ref-type="fig" rid="pharmaceuticals-12-00146-f001">Figure 1</xref>). Phages exhibited various plaque morphologies, varying from very small (less than 0.5 mm diameter) to large (up to 4 mm diameter). Plaques were formed on agar plates with <italic>E. coli </italic>host that was used to isolate the phages.</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1"></th><th colspan="6" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">The Composite Sustainability Indicator (CSI)</th><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Average Score<sup>①</sup></th><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Growth Rate<sup>②</sup></th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2011</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2012</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2013</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2014</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2015</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2016</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Beijing</td><td align="center" valign="middle" rowspan="1" colspan="1">0.565</td><td align="center" valign="middle" rowspan="1" colspan="1">0.59</td><td align="center" valign="middle" rowspan="1" colspan="1">0.609</td><td align="center" valign="middle" rowspan="1" colspan="1">0.605</td><td align="center" valign="middle" rowspan="1" colspan="1">0.588</td><td align="center" valign="middle" rowspan="1" colspan="1">0.634</td><td align="center" valign="middle" rowspan="1" colspan="1">0.598</td><td align="center" valign="middle" rowspan="1" colspan="1">2.44%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tianjin</td><td align="center" valign="middle" rowspan="1" colspan="1">0.562</td><td align="center" valign="middle" rowspan="1" colspan="1">0.555</td><td align="center" valign="middle" rowspan="1" colspan="1">0.553</td><td align="center" valign="middle" rowspan="1" colspan="1">0.513</td><td align="center" valign="middle" rowspan="1" colspan="1">0.522</td><td align="center" valign="middle" rowspan="1" colspan="1">0.515</td><td align="center" valign="middle" rowspan="1" colspan="1">0.537</td><td align="center" valign="middle" rowspan="1" colspan="1">−1.66%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hebei</td><td align="center" valign="middle" rowspan="1" colspan="1">0.403</td><td align="center" valign="middle" rowspan="1" colspan="1">0.401</td><td align="center" valign="middle" rowspan="1" colspan="1">0.414</td><td align="center" valign="middle" rowspan="1" colspan="1">0.426</td><td align="center" valign="middle" rowspan="1" colspan="1">0.467</td><td align="center" valign="middle" rowspan="1" colspan="1">0.503</td><td align="center" valign="middle" rowspan="1" colspan="1">0.436</td><td align="center" valign="middle" rowspan="1" colspan="1">4.93%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Shanxi</td><td align="center" valign="middle" rowspan="1" colspan="1">0.407</td><td align="center" valign="middle" rowspan="1" colspan="1">0.419</td><td align="center" valign="middle" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" rowspan="1" colspan="1">0.434</td><td align="center" valign="middle" rowspan="1" colspan="1">0.437</td><td align="center" valign="middle" rowspan="1" colspan="1">0.482</td><td align="center" valign="middle" rowspan="1" colspan="1">0.437</td><td align="center" valign="middle" rowspan="1" colspan="1">3.70%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Inner Mongolia</td><td align="center" valign="middle" rowspan="1" colspan="1">0.522</td><td align="center" valign="middle" rowspan="1" colspan="1">0.523</td><td align="center" valign="middle" rowspan="1" colspan="1">0.532</td><td align="center" valign="middle" rowspan="1" colspan="1">0.556</td><td align="center" valign="middle" rowspan="1" colspan="1">0.558</td><td align="center" valign="middle" rowspan="1" colspan="1">0.598</td><td align="center" valign="middle" rowspan="1" colspan="1">0.548</td><td align="center" valign="middle" rowspan="1" colspan="1">2.89%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Liaoning</td><td align="center" valign="middle" rowspan="1" colspan="1">0.474</td><td align="center" valign="middle" rowspan="1" colspan="1">0.486</td><td align="center" valign="middle" rowspan="1" colspan="1">0.515</td><td align="center" valign="middle" rowspan="1" colspan="1">0.509</td><td align="center" valign="middle" rowspan="1" colspan="1">0.509</td><td align="center" valign="middle" rowspan="1" colspan="1">0.453</td><td align="center" valign="middle" rowspan="1" colspan="1">0.491</td><td align="center" valign="middle" rowspan="1" colspan="1">−0.91%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Jilin</td><td align="center" valign="middle" rowspan="1" colspan="1">0.406</td><td align="center" valign="middle" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" rowspan="1" colspan="1">0.455</td><td align="center" valign="middle" rowspan="1" colspan="1">0.466</td><td align="center" valign="middle" rowspan="1" colspan="1">0.467</td><td align="center" valign="middle" rowspan="1" colspan="1">0.517</td><td align="center" valign="middle" rowspan="1" colspan="1">0.459</td><td align="center" valign="middle" rowspan="1" colspan="1">5.46%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Heilongjiang</td><td align="center" valign="middle" rowspan="1" colspan="1">0.393</td><td align="center" valign="middle" rowspan="1" colspan="1">0.397</td><td align="center" valign="middle" rowspan="1" colspan="1">0.432</td><td align="center" valign="middle" rowspan="1" colspan="1">0.431</td><td align="center" valign="middle" rowspan="1" colspan="1">0.432</td><td align="center" valign="middle" rowspan="1" colspan="1">0.46</td><td align="center" valign="middle" rowspan="1" colspan="1">0.424</td><td align="center" valign="middle" rowspan="1" colspan="1">3.42%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Shanghai</td><td align="center" valign="middle" rowspan="1" colspan="1">0.45</td><td align="center" valign="middle" rowspan="1" colspan="1">0.455</td><td align="center" valign="middle" rowspan="1" colspan="1">0.449</td><td align="center" valign="middle" rowspan="1" colspan="1">0.477</td><td align="center" valign="middle" rowspan="1" colspan="1">0.496</td><td align="center" valign="middle" rowspan="1" colspan="1">0.556</td><td align="center" valign="middle" rowspan="1" colspan="1">0.48</td><td align="center" valign="middle" rowspan="1" colspan="1">4.69%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Jiangsu</td><td align="center" valign="middle" rowspan="1" colspan="1">0.53</td><td align="center" valign="middle" rowspan="1" colspan="1">0.517</td><td align="center" valign="middle" rowspan="1" colspan="1">0.555</td><td align="center" valign="middle" rowspan="1" colspan="1">0.547</td><td align="center" valign="middle" rowspan="1" colspan="1">0.566</td><td align="center" valign="middle" rowspan="1" colspan="1">0.586</td><td align="center" valign="middle" rowspan="1" colspan="1">0.55</td><td align="center" valign="middle" rowspan="1" colspan="1">2.11%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Zhejiang</td><td align="center" valign="middle" rowspan="1" colspan="1">0.534</td><td align="center" valign="middle" rowspan="1" colspan="1">0.545</td><td align="center" valign="middle" rowspan="1" colspan="1">0.576</td><td align="center" valign="middle" rowspan="1" colspan="1">0.588</td><td align="center" valign="middle" rowspan="1" colspan="1">0.594</td><td align="center" valign="middle" rowspan="1" colspan="1">0.613</td><td align="center" valign="middle" rowspan="1" colspan="1">0.575</td><td align="center" valign="middle" rowspan="1" colspan="1">2.96%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Anhui</td><td align="center" valign="middle" rowspan="1" colspan="1">0.412</td><td align="center" valign="middle" rowspan="1" colspan="1">0.43</td><td align="center" valign="middle" rowspan="1" colspan="1">0.503</td><td align="center" valign="middle" rowspan="1" colspan="1">0.483</td><td align="center" valign="middle" rowspan="1" colspan="1">0.51</td><td align="center" valign="middle" rowspan="1" colspan="1">0.582</td><td align="center" valign="middle" rowspan="1" colspan="1">0.486</td><td align="center" valign="middle" rowspan="1" colspan="1">8.25%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Fujian</td><td align="center" valign="middle" rowspan="1" colspan="1">0.487</td><td align="center" valign="middle" rowspan="1" colspan="1">0.525</td><td align="center" valign="middle" rowspan="1" colspan="1">0.537</td><td align="center" valign="middle" rowspan="1" colspan="1">0.547</td><td align="center" valign="middle" rowspan="1" colspan="1">0.574</td><td align="center" valign="middle" rowspan="1" colspan="1">0.586</td><td align="center" valign="middle" rowspan="1" colspan="1">0.543</td><td align="center" valign="middle" rowspan="1" colspan="1">4.03%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Jiangxi</td><td align="center" valign="middle" rowspan="1" colspan="1">0.403</td><td align="center" valign="middle" rowspan="1" colspan="1">0.42</td><td align="center" valign="middle" rowspan="1" colspan="1">0.45</td><td align="center" valign="middle" rowspan="1" colspan="1">0.423</td><td align="center" valign="middle" rowspan="1" colspan="1">0.45</td><td align="center" valign="middle" rowspan="1" colspan="1">0.507</td><td align="center" valign="middle" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" rowspan="1" colspan="1">5.20%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Shandong</td><td align="center" valign="middle" rowspan="1" colspan="1">0.537</td><td align="center" valign="middle" rowspan="1" colspan="1">0.537</td><td align="center" valign="middle" rowspan="1" colspan="1">0.572</td><td align="center" valign="middle" rowspan="1" colspan="1">0.574</td><td align="center" valign="middle" rowspan="1" colspan="1">0.561</td><td align="center" valign="middle" rowspan="1" colspan="1">0.588</td><td align="center" valign="middle" rowspan="1" colspan="1">0.561</td><td align="center" valign="middle" rowspan="1" colspan="1">1.90%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Henan</td><td align="center" valign="middle" rowspan="1" colspan="1">0.33</td><td align="center" valign="middle" rowspan="1" colspan="1">0.337</td><td align="center" valign="middle" rowspan="1" colspan="1">0.351</td><td align="center" valign="middle" rowspan="1" colspan="1">0.382</td><td align="center" valign="middle" rowspan="1" colspan="1">0.402</td><td align="center" valign="middle" rowspan="1" colspan="1">0.484</td><td align="center" valign="middle" rowspan="1" colspan="1">0.381</td><td align="center" valign="middle" rowspan="1" colspan="1">9.30%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hubei</td><td align="center" valign="middle" rowspan="1" colspan="1">0.421</td><td align="center" valign="middle" rowspan="1" colspan="1">0.446</td><td align="center" valign="middle" rowspan="1" colspan="1">0.458</td><td align="center" valign="middle" rowspan="1" colspan="1">0.501</td><td align="center" valign="middle" rowspan="1" colspan="1">0.518</td><td align="center" valign="middle" rowspan="1" colspan="1">0.574</td><td align="center" valign="middle" rowspan="1" colspan="1">0.486</td><td align="center" valign="middle" rowspan="1" colspan="1">7.27%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hunan</td><td align="center" valign="middle" rowspan="1" colspan="1">0.398</td><td align="center" valign="middle" rowspan="1" colspan="1">0.431</td><td align="center" valign="middle" rowspan="1" colspan="1">0.433</td><td align="center" valign="middle" rowspan="1" colspan="1">0.464</td><td align="center" valign="middle" rowspan="1" colspan="1">0.508</td><td align="center" valign="middle" rowspan="1" colspan="1">0.551</td><td align="center" valign="middle" rowspan="1" colspan="1">0.464</td><td align="center" valign="middle" rowspan="1" colspan="1">7.70%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Guangdong</td><td align="center" valign="middle" rowspan="1" colspan="1">0.474</td><td align="center" valign="middle" rowspan="1" colspan="1">0.451</td><td align="center" valign="middle" rowspan="1" colspan="1">0.482</td><td align="center" valign="middle" rowspan="1" colspan="1">0.471</td><td align="center" valign="middle" rowspan="1" colspan="1">0.514</td><td align="center" valign="middle" rowspan="1" colspan="1">0.534</td><td align="center" valign="middle" rowspan="1" colspan="1">0.488</td><td align="center" valign="middle" rowspan="1" colspan="1">2.54%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Guangxi</td><td align="center" valign="middle" rowspan="1" colspan="1">0.415</td><td align="center" valign="middle" rowspan="1" colspan="1">0.431</td><td align="center" valign="middle" rowspan="1" colspan="1">0.436</td><td align="center" valign="middle" rowspan="1" colspan="1">0.443</td><td align="center" valign="middle" rowspan="1" colspan="1">0.477</td><td align="center" valign="middle" rowspan="1" colspan="1">0.522</td><td align="center" valign="middle" rowspan="1" colspan="1">0.454</td><td align="center" valign="middle" rowspan="1" colspan="1">5.18%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hainan</td><td align="center" valign="middle" rowspan="1" colspan="1">0.547</td><td align="center" valign="middle" rowspan="1" colspan="1">0.596</td><td align="center" valign="middle" rowspan="1" colspan="1">0.595</td><td align="center" valign="middle" rowspan="1" colspan="1">0.585</td><td align="center" valign="middle" rowspan="1" colspan="1">0.569</td><td align="center" valign="middle" rowspan="1" colspan="1">0.598</td><td align="center" valign="middle" rowspan="1" colspan="1">0.582</td><td align="center" valign="middle" rowspan="1" colspan="1">1.87%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chongqing</td><td align="center" valign="middle" rowspan="1" colspan="1">0.496</td><td align="center" valign="middle" rowspan="1" colspan="1">0.531</td><td align="center" valign="middle" rowspan="1" colspan="1">0.541</td><td align="center" valign="middle" rowspan="1" colspan="1">0.571</td><td align="center" valign="middle" rowspan="1" colspan="1">0.572</td><td align="center" valign="middle" rowspan="1" colspan="1">0.604</td><td align="center" valign="middle" rowspan="1" colspan="1">0.553</td><td align="center" valign="middle" rowspan="1" colspan="1">4.36%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Sichuan</td><td align="center" valign="middle" rowspan="1" colspan="1">0.388</td><td align="center" valign="middle" rowspan="1" colspan="1">0.401</td><td align="center" valign="middle" rowspan="1" colspan="1">0.407</td><td align="center" valign="middle" rowspan="1" colspan="1">0.417</td><td align="center" valign="middle" rowspan="1" colspan="1">0.46</td><td align="center" valign="middle" rowspan="1" colspan="1">0.512</td><td align="center" valign="middle" rowspan="1" colspan="1">0.431</td><td align="center" valign="middle" rowspan="1" colspan="1">6.41%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Guizhou</td><td align="center" valign="middle" rowspan="1" colspan="1">0.393</td><td align="center" valign="middle" rowspan="1" colspan="1">0.427</td><td align="center" valign="middle" rowspan="1" colspan="1">0.422</td><td align="center" valign="middle" rowspan="1" colspan="1">0.452</td><td align="center" valign="middle" rowspan="1" colspan="1">0.473</td><td align="center" valign="middle" rowspan="1" colspan="1">0.518</td><td align="center" valign="middle" rowspan="1" colspan="1">0.448</td><td align="center" valign="middle" rowspan="1" colspan="1">6.35%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Yunnan</td><td align="center" valign="middle" rowspan="1" colspan="1">0.427</td><td align="center" valign="middle" rowspan="1" colspan="1">0.432</td><td align="center" valign="middle" rowspan="1" colspan="1">0.446</td><td align="center" valign="middle" rowspan="1" colspan="1">0.457</td><td align="center" valign="middle" rowspan="1" colspan="1">0.449</td><td align="center" valign="middle" rowspan="1" colspan="1">0.504</td><td align="center" valign="middle" rowspan="1" colspan="1">0.452</td><td align="center" valign="middle" rowspan="1" colspan="1">3.58%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tibet</td><td align="center" valign="middle" rowspan="1" colspan="1">0.534</td><td align="center" valign="middle" rowspan="1" colspan="1">0.55</td><td align="center" valign="middle" rowspan="1" colspan="1">0.56</td><td align="center" valign="middle" rowspan="1" colspan="1">0.582</td><td align="center" valign="middle" rowspan="1" colspan="1">0.582</td><td align="center" valign="middle" rowspan="1" colspan="1">0.558</td><td align="center" valign="middle" rowspan="1" colspan="1">0.561</td><td align="center" valign="middle" rowspan="1" colspan="1">0.92%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Shaanxi</td><td align="center" valign="middle" rowspan="1" colspan="1">0.483</td><td align="center" valign="middle" rowspan="1" colspan="1">0.521</td><td align="center" valign="middle" rowspan="1" colspan="1">0.532</td><td align="center" valign="middle" rowspan="1" colspan="1">0.526</td><td align="center" valign="middle" rowspan="1" colspan="1">0.545</td><td align="center" valign="middle" rowspan="1" colspan="1">0.568</td><td align="center" valign="middle" rowspan="1" colspan="1">0.529</td><td align="center" valign="middle" rowspan="1" colspan="1">3.53%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Gansu</td><td align="center" valign="middle" rowspan="1" colspan="1">0.421</td><td align="center" valign="middle" rowspan="1" colspan="1">0.429</td><td align="center" valign="middle" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" rowspan="1" colspan="1">0.43</td><td align="center" valign="middle" rowspan="1" colspan="1">0.474</td><td align="center" valign="middle" rowspan="1" colspan="1">0.44</td><td align="center" valign="middle" rowspan="1" colspan="1">2.49%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Qinghai</td><td align="center" valign="middle" rowspan="1" colspan="1">0.476</td><td align="center" valign="middle" rowspan="1" colspan="1">0.485</td><td align="center" valign="middle" rowspan="1" colspan="1">0.49</td><td align="center" valign="middle" rowspan="1" colspan="1">0.504</td><td align="center" valign="middle" rowspan="1" colspan="1">0.502</td><td align="center" valign="middle" rowspan="1" colspan="1">0.549</td><td align="center" valign="middle" rowspan="1" colspan="1">0.501</td><td align="center" valign="middle" rowspan="1" colspan="1">3.06%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ningxia</td><td align="center" valign="middle" rowspan="1" colspan="1">0.457</td><td align="center" valign="middle" rowspan="1" colspan="1">0.481</td><td align="center" valign="middle" rowspan="1" colspan="1">0.501</td><td align="center" valign="middle" rowspan="1" colspan="1">0.512</td><td align="center" valign="middle" rowspan="1" colspan="1">0.503</td><td align="center" valign="middle" rowspan="1" colspan="1">0.551</td><td align="center" valign="middle" rowspan="1" colspan="1">0.501</td><td align="center" valign="middle" rowspan="1" colspan="1">4.15%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Xinjiang</td><td align="center" valign="middle" rowspan="1" colspan="1">0.5</td><td align="center" valign="middle" rowspan="1" colspan="1">0.494</td><td align="center" valign="middle" rowspan="1" colspan="1">0.498</td><td align="center" valign="middle" rowspan="1" colspan="1">0.515</td><td align="center" valign="middle" rowspan="1" colspan="1">0.546</td><td align="center" valign="middle" rowspan="1" colspan="1">0.567</td><td align="center" valign="middle" rowspan="1" colspan="1">0.52</td><td align="center" valign="middle" rowspan="1" colspan="1">2.68%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">East China<sup>③</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">0.509</td><td align="center" valign="middle" rowspan="1" colspan="1">0.517</td><td align="center" valign="middle" rowspan="1" colspan="1">0.534</td><td align="center" valign="middle" rowspan="1" colspan="1">0.533</td><td align="center" valign="middle" rowspan="1" colspan="1">0.545</td><td align="center" valign="middle" rowspan="1" colspan="1">0.571</td><td align="center" valign="middle" rowspan="1" colspan="1">0.535</td><td align="center" valign="middle" rowspan="1" colspan="1">2.45%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Middle China</td><td align="center" valign="middle" rowspan="1" colspan="1">0.395</td><td align="center" valign="middle" rowspan="1" colspan="1">0.414</td><td align="center" valign="middle" rowspan="1" colspan="1">0.439</td><td align="center" valign="middle" rowspan="1" colspan="1">0.448</td><td align="center" valign="middle" rowspan="1" colspan="1">0.471</td><td align="center" valign="middle" rowspan="1" colspan="1">0.53</td><td align="center" valign="middle" rowspan="1" colspan="1">0.449</td><td align="center" valign="middle" rowspan="1" colspan="1">6.83%</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">West China</td><td align="center" valign="middle" rowspan="1" colspan="1">0.459</td><td align="center" valign="middle" rowspan="1" colspan="1">0.475</td><td align="center" valign="middle" rowspan="1" colspan="1">0.484</td><td align="center" valign="middle" rowspan="1" colspan="1">0.498</td><td align="center" valign="middle" rowspan="1" colspan="1">0.508</td><td align="center" valign="middle" rowspan="1" colspan="1">0.544</td><td align="center" valign="middle" rowspan="1" colspan="1">0.495</td><td align="center" valign="middle" rowspan="1" colspan="1">3.68%</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Northeastern China</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.424</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.442</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.467</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.469</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.469</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.477</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.458</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2.46%</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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