Abnormal activity of corneal cold thermoreceptors underlies the unpleasant sensations in dry eye disease
Identifieur interne : 000386 ( Ncbi/Merge ); précédent : 000385; suivant : 000387Abnormal activity of corneal cold thermoreceptors underlies the unpleasant sensations in dry eye disease
Auteurs : Illés Kovács [Espagne, Hongrie] ; Carolina Luna [Espagne] ; Susana Quirce [Espagne] ; Kamila Mizerska [Espagne] ; Gerard Callejo [Espagne] ; Ana Riestra [Espagne] ; Laura Fernández-Sánchez [Espagne] ; Victor M. Meseguer [Espagne] ; Nicolás Cuenca [Espagne] ; Jesús Merayo-Lloves [Espagne] ; M. Carmen Acosta [Espagne] ; Xavier Gasull [Espagne] ; Carlos Belmonte [Espagne] ; Juana Gallar [Espagne]Source :
- Pain [ 0304-3959 ] ; 2015.
Abstract
Discomfort in dry eye is possibly caused by an augmented ongoing activity in corneal cold neurons secondary to dryness-induced alterations in sodium and potassium channel expression.
Url:
DOI: 10.1097/j.pain.0000000000000455
PubMed: 26675826
PubMed Central: 4733818
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Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2">Department of Ophthalmology, Semmelweis University, Budapest, Hungary</nlm:aff><country xml:lang="fr">Hongrie</country><wicri:regionArea>Department of Ophthalmology, Semmelweis University, Budapest</wicri:regionArea><placeName><settlement type="city">Budapest</settlement><region nuts="2">Hongrie centrale</region></placeName></affiliation></author><author><name sortKey="Luna, Carolina" sort="Luna, Carolina" uniqKey="Luna C" first="Carolina" last="Luna">Carolina Luna</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author><author><name sortKey="Quirce, Susana" sort="Quirce, Susana" uniqKey="Quirce S" first="Susana" last="Quirce">Susana Quirce</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author><author><name sortKey="Mizerska, Kamila" sort="Mizerska, Kamila" uniqKey="Mizerska K" first="Kamila" last="Mizerska">Kamila Mizerska</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author><author><name sortKey="Callejo, Gerard" sort="Callejo, Gerard" uniqKey="Callejo G" first="Gerard" last="Callejo">Gerard Callejo</name><affiliation wicri:level="3"><nlm:aff id="aff3">Laboratory of Neurophysiology, Department of Biomedicine, School of Medicine, University of Barcelona, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Laboratory of Neurophysiology, Department of Biomedicine, School of Medicine, University of Barcelona, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4">Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author><author><name sortKey="Riestra, Ana" sort="Riestra, Ana" uniqKey="Riestra A" first="Ana" last="Riestra">Ana Riestra</name><affiliation wicri:level="1"><nlm:aff id="aff5">Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo</wicri:regionArea><wicri:noRegion>Oviedo</wicri:noRegion></affiliation></author><author><name sortKey="Fernandez Sanchez, Laura" sort="Fernandez Sanchez, Laura" uniqKey="Fernandez Sanchez L" first="Laura" last="Fernández-Sánchez">Laura Fernández-Sánchez</name><affiliation wicri:level="4"><nlm:aff id="aff6">Departamento de Fisiología, Genética y Microbiología, Universidad de Alicante, San Vicente del Raspeig, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departamento de Fisiología, Genética y Microbiología, Universidad de Alicante, San Vicente del Raspeig</wicri:regionArea><orgName type="university">Université d'Alicante</orgName><placeName><settlement type="city">Alicante</settlement><region nuts="2" type="region">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Meseguer, Victor M" sort="Meseguer, Victor M" uniqKey="Meseguer V" first="Victor M." last="Meseguer">Victor M. Meseguer</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author><author><name sortKey="Cuenca, Nicolas" sort="Cuenca, Nicolas" uniqKey="Cuenca N" first="Nicolás" last="Cuenca">Nicolás Cuenca</name><affiliation wicri:level="4"><nlm:aff id="aff6">Departamento de Fisiología, Genética y Microbiología, Universidad de Alicante, San Vicente del Raspeig, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departamento de Fisiología, Genética y Microbiología, Universidad de Alicante, San Vicente del Raspeig</wicri:regionArea><orgName type="university">Université d'Alicante</orgName><placeName><settlement type="city">Alicante</settlement><region nuts="2" type="region">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Merayo Lloves, Jesus" sort="Merayo Lloves, Jesus" uniqKey="Merayo Lloves J" first="Jesús" last="Merayo-Lloves">Jesús Merayo-Lloves</name><affiliation wicri:level="1"><nlm:aff id="aff5">Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo</wicri:regionArea><wicri:noRegion>Oviedo</wicri:noRegion></affiliation></author><author><name sortKey="Acosta, M Carmen" sort="Acosta, M Carmen" uniqKey="Acosta M" first="M. Carmen" last="Acosta">M. Carmen Acosta</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author><author><name sortKey="Gasull, Xavier" sort="Gasull, Xavier" uniqKey="Gasull X" first="Xavier" last="Gasull">Xavier Gasull</name><affiliation wicri:level="3"><nlm:aff id="aff3">Laboratory of Neurophysiology, Department of Biomedicine, School of Medicine, University of Barcelona, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Laboratory of Neurophysiology, Department of Biomedicine, School of Medicine, University of Barcelona, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4">Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author><author><name sortKey="Belmonte, Carlos" sort="Belmonte, Carlos" uniqKey="Belmonte C" first="Carlos" last="Belmonte">Carlos Belmonte</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5">Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo</wicri:regionArea><wicri:noRegion>Oviedo</wicri:noRegion></affiliation></author><author><name sortKey="Gallar, Juana" sort="Gallar, Juana" uniqKey="Gallar J" first="Juana" last="Gallar">Juana Gallar</name><affiliation wicri:level="1"><nlm:aff id="aff1">Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante</wicri:regionArea><wicri:noRegion>San Juan de Alicante</wicri:noRegion></affiliation></author></analytic><series><title level="j">Pain</title><idno type="ISSN">0304-3959</idno><idno type="eISSN">1872-6623</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Discomfort in dry eye is possibly caused by an augmented ongoing activity in corneal cold neurons secondary to dryness-induced alterations in sodium and potassium channel expression.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abdulla, Fa" uniqKey="Abdulla F">FA Abdulla</name></author><author><name sortKey="Smith, Pa" uniqKey="Smith P">PA Smith</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Abdulla, Fa" uniqKey="Abdulla F">FA Abdulla</name></author><author><name sortKey="Smith, Pa" uniqKey="Smith P">PA 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Pain</journal-id><journal-id journal-id-type="iso-abbrev">Pain</journal-id><journal-id journal-id-type="coden">JPAIN</journal-id><journal-id journal-id-type="pmc">Pain</journal-id><journal-id journal-id-type="publisher-id">JOP</journal-id><journal-title-group><journal-title>Pain</journal-title></journal-title-group><issn pub-type="ppub">0304-3959</issn><issn pub-type="epub">1872-6623</issn><publisher><publisher-name>Wolters Kluwer</publisher-name><publisher-loc>Philadelphia, PA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26675826</article-id><article-id pub-id-type="pmc">4733818</article-id><article-id pub-id-type="publisher-id">PAIN-D-14-14169</article-id><article-id pub-id-type="doi">10.1097/j.pain.0000000000000455</article-id><article-id pub-id-type="art-access-id">00016</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Paper</subject></subj-group></article-categories><title-group><article-title>Abnormal activity of corneal cold thermoreceptors underlies the unpleasant sensations in dry eye disease</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Kovács</surname><given-names>Illés</given-names></name><xref ref-type="aff" rid="aff1">a</xref><xref ref-type="aff" rid="aff2">b</xref></contrib><contrib contrib-type="author"><name><surname>Luna</surname><given-names>Carolina</given-names></name><xref ref-type="aff" rid="aff1">a</xref></contrib><contrib contrib-type="author"><name><surname>Quirce</surname><given-names>Susana</given-names></name><xref ref-type="aff" rid="aff1">a</xref></contrib><contrib contrib-type="author"><name><surname>Mizerska</surname><given-names>Kamila</given-names></name><xref ref-type="aff" rid="aff1">a</xref></contrib><contrib contrib-type="author"><name><surname>Callejo</surname><given-names>Gerard</given-names></name><xref ref-type="aff" rid="aff3">c</xref><xref ref-type="aff" rid="aff4">d</xref></contrib><contrib contrib-type="author"><name><surname>Riestra</surname><given-names>Ana</given-names></name><xref ref-type="aff" rid="aff5">e</xref></contrib><contrib contrib-type="author"><name><surname>Fernández-Sánchez</surname><given-names>Laura</given-names></name><xref ref-type="aff" rid="aff6">f</xref></contrib><contrib contrib-type="author"><name><surname>Meseguer</surname><given-names>Victor M.</given-names></name><xref ref-type="aff" rid="aff1">a</xref></contrib><contrib contrib-type="author"><name><surname>Cuenca</surname><given-names>Nicolás</given-names></name><xref ref-type="aff" rid="aff6">f</xref></contrib><contrib contrib-type="author"><name><surname>Merayo-Lloves</surname><given-names>Jesús</given-names></name><xref ref-type="aff" rid="aff5">e</xref></contrib><contrib contrib-type="author"><name><surname>Acosta</surname><given-names>M. Carmen</given-names></name><xref ref-type="aff" rid="aff1">a</xref></contrib><contrib contrib-type="author"><name><surname>Gasull</surname><given-names>Xavier</given-names></name><xref ref-type="aff" rid="aff3">c</xref><xref ref-type="aff" rid="aff4">d</xref></contrib><contrib contrib-type="author"><name><surname>Belmonte</surname><given-names>Carlos</given-names></name><xref ref-type="aff" rid="aff1">a</xref><xref ref-type="aff" rid="aff5">e</xref></contrib><contrib contrib-type="author"><name><surname>Gallar</surname><given-names>Juana</given-names></name><xref ref-type="aff" rid="aff1">a</xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><aff id="aff1"><label>a</label>Instituto de Neurociencias, Universidad Miguel Hernández–CSIC, San Juan de Alicante, Spain</aff><aff id="aff2"><label>b</label>Department of Ophthalmology, Semmelweis University, Budapest, Hungary</aff><aff id="aff3"><label>c</label>Laboratory of Neurophysiology, Department of Biomedicine, School of Medicine, University of Barcelona, Barcelona, Spain</aff><aff id="aff4"><label>d</label>Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain</aff><aff id="aff5"><label>e</label>Instituto Universitario Fernández-Vega, Universidad de Oviedo and Fundación de Investigación Oftalmológica, Oviedo, Spain</aff><aff id="aff6"><label>f</label>Departamento de Fisiología, Genética y Microbiología, Universidad de Alicante, San Vicente del Raspeig, Spain</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Corresponding author. Address: Instituto de Neurociencias, Universidad Miguel Hernández-CSIC, Avenida Santiago Ramon y Cajal, s/n, 03550 San Juan de Alicante, Spain. Tel.: +34 965919532; fax: +34 965919549. E-mail address: <email>juana.gallar@umh.es</email> (J. Gallar).</corresp></author-notes><pub-date pub-type="epub"><day>15</day><month>12</month><year>2015</year></pub-date><pub-date pub-type="ppub"><month>2</month><year>2016</year></pub-date><volume>157</volume><issue>2</issue><fpage>399</fpage><lpage>417</lpage><history><date date-type="received"><day>01</day><month>9</month><year>2015</year></date><date date-type="rev-recd"><day>09</day><month>10</month><year>2015</year></date><date date-type="accepted"><day>28</day><month>10</month><year>2015</year></date></history><permissions><copyright-statement>© 2015 International Association for the Study of Pain</copyright-statement><copyright-year>2015</copyright-year></permissions><self-uri xlink:type="simple" xlink:href="jop-157-399.pdf"></self-uri><abstract abstract-type="toc"><p>Discomfort in dry eye is possibly caused by an augmented ongoing activity in corneal cold neurons secondary to dryness-induced alterations in sodium and potassium channel expression.</p></abstract><abstract><title>Abstract</title><p>Dry eye disease (DED) affects >10% of the population worldwide, and it provokes an unpleasant sensation of ocular dryness, whose underlying neural mechanisms remain unknown. Removal of the main lachrymal gland in guinea pigs caused long-term reduction of basal tearing accompanied by changes in the architecture and density of subbasal corneal nerves and epithelial terminals. After 4 weeks, ongoing impulse activity and responses to cooling of corneal cold thermoreceptor endings were enhanced. Menthol (200 μM) first excited and then inactivated this augmented spontaneous and cold-evoked activity. Comparatively, corneal polymodal nociceptors of tear-deficient eyes remained silent and exhibited only a mild sensitization to acidic stimulation, whereas mechanonociceptors were not affected. Dryness-induced changes in peripheral cold thermoreceptor responsiveness developed in parallel with a progressive excitability enhancement of corneal cold trigeminal ganglion neurons, primarily due to an increase of sodium currents and a decrease of potassium currents. In corneal polymodal nociceptor neurons, sodium currents were enhanced whereas potassium currents remain unaltered. In healthy humans, exposure of the eye surface to menthol vapors or to cold air currents evoked unpleasant sensations accompanied by increased blinking frequency that we attributed to cold thermoreceptor stimulation. Notably, stimulation with menthol reduced the ongoing background discomfort of patients with DED, conceivably due to use-dependent inactivation of cold thermoreceptors. Together, these data indicate that cold thermoreceptors contribute importantly to the detection and signaling of ocular surface wetness, and develop under chronic eye dryness conditions an injury-evoked neuropathic firing that seems to underlie the unpleasant sensations experienced by patients with DED.</p></abstract><kwd-group><title>Keywords:</title><kwd>Eye pain</kwd><kwd>Dry eye</kwd><kwd>Corneal nerve injury</kwd><kwd>Neuropathic pain</kwd><kwd>Eye inflammation</kwd><kwd>Cold thermoreceptors</kwd><kwd>Nociceptors</kwd></kwd-group></article-meta></front></pmc><affiliations><list><country><li>Espagne</li><li>Hongrie</li></country><region><li>Catalogne</li><li>Communauté valencienne</li><li>Hongrie centrale</li></region><settlement><li>Alicante</li><li>Barcelone</li><li>Budapest</li></settlement><orgName><li>Université d'Alicante</li></orgName></list><tree><country name="Espagne"><noRegion><name sortKey="Kovacs, Illes" sort="Kovacs, Illes" uniqKey="Kovacs I" first="Illés" last="Kovács">Illés Kovács</name></noRegion><name sortKey="Acosta, M Carmen" sort="Acosta, M Carmen" uniqKey="Acosta M" first="M. Carmen" last="Acosta">M. Carmen Acosta</name><name sortKey="Belmonte, Carlos" sort="Belmonte, Carlos" uniqKey="Belmonte C" first="Carlos" last="Belmonte">Carlos Belmonte</name><name sortKey="Belmonte, Carlos" sort="Belmonte, Carlos" uniqKey="Belmonte C" first="Carlos" last="Belmonte">Carlos Belmonte</name><name sortKey="Callejo, Gerard" sort="Callejo, Gerard" uniqKey="Callejo G" first="Gerard" last="Callejo">Gerard Callejo</name><name sortKey="Callejo, Gerard" sort="Callejo, Gerard" uniqKey="Callejo G" first="Gerard" last="Callejo">Gerard Callejo</name><name sortKey="Cuenca, Nicolas" sort="Cuenca, Nicolas" uniqKey="Cuenca N" first="Nicolás" last="Cuenca">Nicolás Cuenca</name><name sortKey="Fernandez Sanchez, Laura" sort="Fernandez Sanchez, Laura" uniqKey="Fernandez Sanchez L" first="Laura" last="Fernández-Sánchez">Laura Fernández-Sánchez</name><name sortKey="Gallar, Juana" sort="Gallar, Juana" uniqKey="Gallar J" first="Juana" last="Gallar">Juana Gallar</name><name sortKey="Gasull, Xavier" sort="Gasull, Xavier" uniqKey="Gasull X" first="Xavier" last="Gasull">Xavier Gasull</name><name sortKey="Gasull, Xavier" sort="Gasull, Xavier" uniqKey="Gasull X" first="Xavier" last="Gasull">Xavier Gasull</name><name sortKey="Luna, Carolina" sort="Luna, Carolina" uniqKey="Luna C" first="Carolina" last="Luna">Carolina Luna</name><name sortKey="Merayo Lloves, Jesus" sort="Merayo Lloves, Jesus" uniqKey="Merayo Lloves J" first="Jesús" last="Merayo-Lloves">Jesús Merayo-Lloves</name><name sortKey="Meseguer, Victor M" sort="Meseguer, Victor M" uniqKey="Meseguer V" first="Victor M." last="Meseguer">Victor M. Meseguer</name><name sortKey="Mizerska, Kamila" sort="Mizerska, Kamila" uniqKey="Mizerska K" first="Kamila" last="Mizerska">Kamila Mizerska</name><name sortKey="Quirce, Susana" sort="Quirce, Susana" uniqKey="Quirce S" first="Susana" last="Quirce">Susana Quirce</name><name sortKey="Riestra, Ana" sort="Riestra, Ana" uniqKey="Riestra A" first="Ana" last="Riestra">Ana Riestra</name></country><country name="Hongrie"><region name="Hongrie centrale"><name sortKey="Kovacs, Illes" sort="Kovacs, Illes" uniqKey="Kovacs I" first="Illés" last="Kovács">Illés Kovács</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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