Comparison of silver nanoparticles stored under air or argon with respect to the induction of intracellular free radicals and toxic effects toward keratinocytes.
Identifieur interne : 000822 ( Main/Corpus ); précédent : 000821; suivant : 000823Comparison of silver nanoparticles stored under air or argon with respect to the induction of intracellular free radicals and toxic effects toward keratinocytes.
Auteurs : Sebastian Ahlberg ; Martina C. Meinke ; Luise Werner ; Matthias Epple ; Joerg Diendorf ; Ulrike Blume-Peytavi ; Juergen Lademann ; Annika Vogt ; Fiorenza RancanSource :
- European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V [ 1873-3441 ] ; 2014.
English descriptors
- KwdEn :
- Air (MeSH), Anti-Bacterial Agents (chemistry), Anti-Bacterial Agents (pharmacokinetics), Anti-Bacterial Agents (toxicity), Apoptosis (drug effects), Argon (chemistry), Cell Culture Techniques (MeSH), Cell Line (MeSH), Dose-Response Relationship, Drug (MeSH), Drug Storage (methods), Free Radicals (metabolism), Humans (MeSH), Keratinocytes (drug effects), Keratinocytes (metabolism), Keratinocytes (ultrastructure), Metal Nanoparticles (chemistry), Microscopy, Electron, Transmission (MeSH), Particle Size (MeSH), Silver (chemistry), Silver (pharmacokinetics), Silver (toxicity).
- MESH :
- chemical , chemistry : Anti-Bacterial Agents, Argon, Silver.
- chemical , metabolism : Free Radicals.
- chemical , pharmacokinetics : Anti-Bacterial Agents, Silver.
- chemical , toxicity : Anti-Bacterial Agents, Silver.
- chemistry : Metal Nanoparticles.
- drug effects : Apoptosis, Keratinocytes.
- metabolism : Keratinocytes.
- methods : Drug Storage.
- ultrastructure : Keratinocytes.
- Air, Cell Culture Techniques, Cell Line, Dose-Response Relationship, Drug, Humans, Microscopy, Electron, Transmission, Particle Size.
Abstract
Bacterial infections decreased considerably after the discovery of antibiotics. Nevertheless, because of the rising rate of infections caused by antibiotic-resistant bacteria strains, the search for new bactericidal agents has again become a crucial topic in clinical medicine. Silver nanoparticles (AgNP) have a huge potential in dermatology and wound care management because of their ability to release silver ions (Ag(+) ions) in a prolonged and sustained way. However, negative effects of silver on the patient's cells should not be underestimated. Furthermore, it has been controversially discussed whether AgNP are responsible for nanoparticle-specific outcomes or not. In this study, we investigated the effects of AgNP on human skin keratinocytes (HaCaT) in order to better understand the mechanisms of cytotoxicity and to improve the use of this highly reactive biocide in wound healing. We found that most of the cells with internalized AgNP displayed the typical morphological signs of apoptosis. The cell viability assay (XTT) showed concentration-dependent toxic effects of the AgNP toward HaCaT cells. The generation of reactive oxygen species (ROS) induced by AgNP was investigated in cell suspensions by means of electron paramagnetic resonance (EPR) spectroscopy. In order to distinguish between the effects of Ag(+) ions released during AgNP storage and those of Ag(+) ions released after nanoparticle application, we compared AgNP stored under air (O2) with AgNP stored under argon (Ar). Dispersions of AgNP stored under Ar have a low content of Ag(+) ions because of the absence of oxygen which is needed for oxidative dissolution. The results show that Ag(+) ions released during particle storage are responsible for most of the ROS produced during 1h incubation with the cells. AgNP (Ar) also induced intracellular ROS but to a much smaller extent compared to AgNP (O2). These findings highlight the complexity of experiments to assess the toxicity of AgNP and suggest the possibility of reducing AgNP toxic effects by storing AgNP formulations and even silver-containing wound dressing under an inert gas atmosphere.
DOI: 10.1016/j.ejpb.2014.07.012
PubMed: 25108059
Links to Exploration step
pubmed:25108059Le document en format XML
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Electronic address: fiorenza.rancan@charite.de.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2014">2014</date><idno type="RBID">pubmed:25108059</idno><idno type="pmid">25108059</idno><idno type="doi">10.1016/j.ejpb.2014.07.012</idno><idno type="wicri:Area/Main/Corpus">000822</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000822</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Comparison of silver nanoparticles stored under air or argon with respect to the induction of intracellular free radicals and toxic effects toward keratinocytes.</title><author><name sortKey="Ahlberg, Sebastian" sort="Ahlberg, Sebastian" uniqKey="Ahlberg S" first="Sebastian" last="Ahlberg">Sebastian Ahlberg</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Meinke, Martina C" sort="Meinke, Martina C" uniqKey="Meinke M" first="Martina C" last="Meinke">Martina C. Meinke</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Werner, Luise" sort="Werner, Luise" uniqKey="Werner L" first="Luise" last="Werner">Luise Werner</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Epple, Matthias" sort="Epple, Matthias" uniqKey="Epple M" first="Matthias" last="Epple">Matthias Epple</name><affiliation><nlm:affiliation>Inorganic Chemistry and Center for Nanointegration Duisburg-Essen (CeNIDE), University of Duisburg-Essen, Essen, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Diendorf, Joerg" sort="Diendorf, Joerg" uniqKey="Diendorf J" first="Joerg" last="Diendorf">Joerg Diendorf</name><affiliation><nlm:affiliation>Inorganic Chemistry and Center for Nanointegration Duisburg-Essen (CeNIDE), University of Duisburg-Essen, Essen, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Blume Peytavi, Ulrike" sort="Blume Peytavi, Ulrike" uniqKey="Blume Peytavi U" first="Ulrike" last="Blume-Peytavi">Ulrike Blume-Peytavi</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Lademann, Juergen" sort="Lademann, Juergen" uniqKey="Lademann J" first="Juergen" last="Lademann">Juergen Lademann</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Vogt, Annika" sort="Vogt, Annika" uniqKey="Vogt A" first="Annika" last="Vogt">Annika Vogt</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Rancan, Fiorenza" sort="Rancan, Fiorenza" uniqKey="Rancan F" first="Fiorenza" last="Rancan">Fiorenza Rancan</name><affiliation><nlm:affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany. Electronic address: fiorenza.rancan@charite.de.</nlm:affiliation></affiliation></author></analytic><series><title level="j">European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V</title><idno type="eISSN">1873-3441</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Air (MeSH)</term><term>Anti-Bacterial Agents (chemistry)</term><term>Anti-Bacterial Agents (pharmacokinetics)</term><term>Anti-Bacterial Agents (toxicity)</term><term>Apoptosis (drug effects)</term><term>Argon (chemistry)</term><term>Cell Culture Techniques (MeSH)</term><term>Cell Line (MeSH)</term><term>Dose-Response Relationship, Drug (MeSH)</term><term>Drug Storage (methods)</term><term>Free Radicals (metabolism)</term><term>Humans (MeSH)</term><term>Keratinocytes (drug effects)</term><term>Keratinocytes (metabolism)</term><term>Keratinocytes (ultrastructure)</term><term>Metal Nanoparticles (chemistry)</term><term>Microscopy, Electron, Transmission (MeSH)</term><term>Particle Size (MeSH)</term><term>Silver (chemistry)</term><term>Silver (pharmacokinetics)</term><term>Silver (toxicity)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Anti-Bacterial Agents</term><term>Argon</term><term>Silver</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Free Radicals</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacokinetics" xml:lang="en"><term>Anti-Bacterial Agents</term><term>Silver</term></keywords><keywords scheme="MESH" type="chemical" qualifier="toxicity" xml:lang="en"><term>Anti-Bacterial Agents</term><term>Silver</term></keywords><keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Metal Nanoparticles</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Apoptosis</term><term>Keratinocytes</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Keratinocytes</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Drug Storage</term></keywords><keywords scheme="MESH" qualifier="ultrastructure" xml:lang="en"><term>Keratinocytes</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Air</term><term>Cell Culture Techniques</term><term>Cell Line</term><term>Dose-Response Relationship, Drug</term><term>Humans</term><term>Microscopy, Electron, Transmission</term><term>Particle Size</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Bacterial infections decreased considerably after the discovery of antibiotics. Nevertheless, because of the rising rate of infections caused by antibiotic-resistant bacteria strains, the search for new bactericidal agents has again become a crucial topic in clinical medicine. Silver nanoparticles (AgNP) have a huge potential in dermatology and wound care management because of their ability to release silver ions (Ag(+) ions) in a prolonged and sustained way. However, negative effects of silver on the patient's cells should not be underestimated. Furthermore, it has been controversially discussed whether AgNP are responsible for nanoparticle-specific outcomes or not. In this study, we investigated the effects of AgNP on human skin keratinocytes (HaCaT) in order to better understand the mechanisms of cytotoxicity and to improve the use of this highly reactive biocide in wound healing. We found that most of the cells with internalized AgNP displayed the typical morphological signs of apoptosis. The cell viability assay (XTT) showed concentration-dependent toxic effects of the AgNP toward HaCaT cells. The generation of reactive oxygen species (ROS) induced by AgNP was investigated in cell suspensions by means of electron paramagnetic resonance (EPR) spectroscopy. In order to distinguish between the effects of Ag(+) ions released during AgNP storage and those of Ag(+) ions released after nanoparticle application, we compared AgNP stored under air (O2) with AgNP stored under argon (Ar). Dispersions of AgNP stored under Ar have a low content of Ag(+) ions because of the absence of oxygen which is needed for oxidative dissolution. The results show that Ag(+) ions released during particle storage are responsible for most of the ROS produced during 1h incubation with the cells. AgNP (Ar) also induced intracellular ROS but to a much smaller extent compared to AgNP (O2). These findings highlight the complexity of experiments to assess the toxicity of AgNP and suggest the possibility of reducing AgNP toxic effects by storing AgNP formulations and even silver-containing wound dressing under an inert gas atmosphere.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">25108059</PMID><DateCompleted><Year>2015</Year><Month>07</Month><Day>20</Day></DateCompleted><DateRevised><Year>2014</Year><Month>12</Month><Day>01</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1873-3441</ISSN><JournalIssue CitedMedium="Internet"><Volume>88</Volume><Issue>3</Issue><PubDate><Year>2014</Year><Month>Nov</Month></PubDate></JournalIssue><Title>European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V</Title><ISOAbbreviation>Eur J Pharm Biopharm</ISOAbbreviation></Journal><ArticleTitle>Comparison of silver nanoparticles stored under air or argon with respect to the induction of intracellular free radicals and toxic effects toward keratinocytes.</ArticleTitle><Pagination><MedlinePgn>651-7</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.ejpb.2014.07.012</ELocationID><ELocationID EIdType="pii" ValidYN="Y">S0939-6411(14)00237-9</ELocationID><Abstract><AbstractText>Bacterial infections decreased considerably after the discovery of antibiotics. Nevertheless, because of the rising rate of infections caused by antibiotic-resistant bacteria strains, the search for new bactericidal agents has again become a crucial topic in clinical medicine. Silver nanoparticles (AgNP) have a huge potential in dermatology and wound care management because of their ability to release silver ions (Ag(+) ions) in a prolonged and sustained way. However, negative effects of silver on the patient's cells should not be underestimated. Furthermore, it has been controversially discussed whether AgNP are responsible for nanoparticle-specific outcomes or not. In this study, we investigated the effects of AgNP on human skin keratinocytes (HaCaT) in order to better understand the mechanisms of cytotoxicity and to improve the use of this highly reactive biocide in wound healing. We found that most of the cells with internalized AgNP displayed the typical morphological signs of apoptosis. The cell viability assay (XTT) showed concentration-dependent toxic effects of the AgNP toward HaCaT cells. The generation of reactive oxygen species (ROS) induced by AgNP was investigated in cell suspensions by means of electron paramagnetic resonance (EPR) spectroscopy. In order to distinguish between the effects of Ag(+) ions released during AgNP storage and those of Ag(+) ions released after nanoparticle application, we compared AgNP stored under air (O2) with AgNP stored under argon (Ar). Dispersions of AgNP stored under Ar have a low content of Ag(+) ions because of the absence of oxygen which is needed for oxidative dissolution. The results show that Ag(+) ions released during particle storage are responsible for most of the ROS produced during 1h incubation with the cells. AgNP (Ar) also induced intracellular ROS but to a much smaller extent compared to AgNP (O2). These findings highlight the complexity of experiments to assess the toxicity of AgNP and suggest the possibility of reducing AgNP toxic effects by storing AgNP formulations and even silver-containing wound dressing under an inert gas atmosphere.</AbstractText><CopyrightInformation>Copyright © 2014 Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ahlberg</LastName><ForeName>Sebastian</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meinke</LastName><ForeName>Martina C</ForeName><Initials>MC</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Werner</LastName><ForeName>Luise</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Epple</LastName><ForeName>Matthias</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Inorganic Chemistry and Center for Nanointegration Duisburg-Essen (CeNIDE), University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Diendorf</LastName><ForeName>Joerg</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Inorganic Chemistry and Center for Nanointegration Duisburg-Essen (CeNIDE), University of Duisburg-Essen, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Blume-Peytavi</LastName><ForeName>Ulrike</ForeName><Initials>U</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lademann</LastName><ForeName>Juergen</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vogt</LastName><ForeName>Annika</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rancan</LastName><ForeName>Fiorenza</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Dermatology, Venerology and Allergology, Charité - Universitätsmedizin Berlin, Berlin, Germany. Electronic address: fiorenza.rancan@charite.de.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D003160">Comparative Study</PublicationType><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>08</Month><Day>07</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Eur J Pharm Biopharm</MedlineTA><NlmUniqueID>9109778</NlmUniqueID><ISSNLinking>0939-6411</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000900">Anti-Bacterial Agents</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005609">Free Radicals</NameOfSubstance></Chemical><Chemical><RegistryNumber>3M4G523W1G</RegistryNumber><NameOfSubstance UI="D012834">Silver</NameOfSubstance></Chemical><Chemical><RegistryNumber>67XQY1V3KH</RegistryNumber><NameOfSubstance UI="D001128">Argon</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000388" MajorTopicYN="Y">Air</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000900" MajorTopicYN="N">Anti-Bacterial Agents</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000493" MajorTopicYN="N">pharmacokinetics</QualifierName><QualifierName UI="Q000633" MajorTopicYN="Y">toxicity</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017209" MajorTopicYN="N">Apoptosis</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001128" MajorTopicYN="N">Argon</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018929" MajorTopicYN="N">Cell Culture Techniques</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002460" MajorTopicYN="N">Cell Line</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004305" MajorTopicYN="N">Dose-Response Relationship, Drug</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004356" MajorTopicYN="N">Drug Storage</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005609" MajorTopicYN="N">Free Radicals</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015603" MajorTopicYN="N">Keratinocytes</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D053768" MajorTopicYN="N">Metal Nanoparticles</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D046529" MajorTopicYN="N">Microscopy, Electron, Transmission</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010316" MajorTopicYN="N">Particle Size</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012834" MajorTopicYN="N">Silver</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000493" MajorTopicYN="N">pharmacokinetics</QualifierName><QualifierName UI="Q000633" MajorTopicYN="Y">toxicity</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">AgNP</Keyword><Keyword MajorTopicYN="N">Cellular uptake</Keyword><Keyword MajorTopicYN="N">Cytotoxity</Keyword><Keyword MajorTopicYN="N">Electron paramagnetic resonance spectroscopy</Keyword><Keyword MajorTopicYN="N">Keratinocytes</Keyword><Keyword MajorTopicYN="N">Nanoparticles</Keyword><Keyword MajorTopicYN="N">Skin</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2014</Year><Month>02</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2014</Year><Month>07</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2014</Year><Month>07</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2014</Year><Month>8</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2014</Year><Month>8</Month><Day>12</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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