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class="mw-body-content"><div class="mw-content-ltr mw-parser-output" lang="en" dir="ltr"><div class="shortdescription nomobile noexcerpt noprint searchaux" style="display:none">Mechanism in the respiratory system</div> <style data-mw-deduplicate="TemplateStyles:r1257001546">.mw-parser-output .infobox-subbox{padding:0;border:none;margin:-3px;width:auto;min-width:100%;font-size:100%;clear:none;float:none;background-color:transparent}.mw-parser-output .infobox-3cols-child{margin:auto}.mw-parser-output .infobox .navbar{font-size:100%}@media screen{html.skin-theme-clientpref-night .mw-parser-output .infobox-full-data:not(.notheme)>div:not(.notheme)[style]{background:#1f1f23!important;color:#f8f9fa}}@media screen and (prefers-color-scheme:dark){html.skin-theme-clientpref-os .mw-parser-output .infobox-full-data:not(.notheme) div:not(.notheme){background:#1f1f23!important;color:#f8f9fa}}@media(min-width:640px){body.skin--responsive .mw-parser-output .infobox-table{display:table!important}body.skin--responsive .mw-parser-output .infobox-table>caption{display:table-caption!important}body.skin--responsive .mw-parser-output .infobox-table>tbody{display:table-row-group}body.skin--responsive .mw-parser-output .infobox-table tr{display:table-row!important}body.skin--responsive .mw-parser-output .infobox-table th,body.skin--responsive .mw-parser-output .infobox-table td{padding-left:inherit;padding-right:inherit}}</style><table class="infobox"><tbody><tr><th colspan="2" class="infobox-above" style="background-color:dimgray; color: white">Mucociliary clearance</th></tr><tr><td colspan="2" class="infobox-image"><span class="mw-default-size" typeof="mw:File/Frameless"><a href="/wiki/File:Bronchiolar_epithelium_1_-_SEM.jpg" class="mw-file-description"><img src="//upload.wikimedia.org/wikipedia/commons/thumb/7/78/Bronchiolar_epithelium_1_-_SEM.jpg/250px-Bronchiolar_epithelium_1_-_SEM.jpg" decoding="async" width="250" height="256" class="mw-file-element" srcset="//upload.wikimedia.org/wikipedia/commons/thumb/7/78/Bronchiolar_epithelium_1_-_SEM.jpg/375px-Bronchiolar_epithelium_1_-_SEM.jpg 1.5x, //upload.wikimedia.org/wikipedia/commons/thumb/7/78/Bronchiolar_epithelium_1_-_SEM.jpg/500px-Bronchiolar_epithelium_1_-_SEM.jpg 2x" data-file-width="1024" data-file-height="1049" /></a></span><div class="infobox-caption">Ciliated epithelium in bronchus with short microvilli on non-ciliated cells</div></td></tr><tr><th colspan="2" class="infobox-header" style="background-color: #efefef">Details</th></tr><tr><th scope="row" class="infobox-label" style="padding-right:0.25em"><a href="/wiki/Organ_system" title="Organ system">System</a></th><td class="infobox-data">Respiratory system</td></tr><tr><th colspan="2" class="infobox-header" style="background-color: #efefef">Identifiers</th></tr><tr><th scope="row" class="infobox-label" style="padding-right:0.25em"><a href="/wiki/Medical_Subject_Headings" title="Medical Subject Headings">MeSH</a></th><td class="infobox-data"><a rel="nofollow" class="external text" href="https://meshb.nlm.nih.gov/record/ui?ui=D009079">D009079</a></td></tr><tr><td colspan="2" class="infobox-below"><a href="/wiki/Anatomical_terminology" title="Anatomical terminology">Anatomical terminology</a><div style="text-align: right;"><small class="noprint">[<a href="https://www.wikidata.org/wiki/Q63771488" class="extiw" title="d:Q63771488">edit on Wikidata</a>]</small></div></td></tr></tbody></table> <p><b>Mucociliary clearance</b> (<b>MCC</b>), <b>mucociliary transport</b>, or the <b>mucociliary escalator</b> describes the self-clearing mechanism of the <a href="/wiki/Respiratory_tract" title="Respiratory tract">airways</a> in the <a href="/wiki/Respiratory_system" title="Respiratory system">respiratory system</a>.<sup id="cite_ref-1" class="reference"><a href="#cite_note-1"><span class="cite-bracket">[</span>1<span class="cite-bracket">]</span></a></sup> It is one of the two protective processes for the <a href="/wiki/Lung" title="Lung">lungs</a> in removing inhaled <a href="/wiki/Particulates" title="Particulates">particles</a> including <a href="/wiki/Pathogen" title="Pathogen">pathogens</a> before they can reach the <a href="/wiki/Parenchyma#Lung_parenchyma" title="Parenchyma">delicate tissue</a> of the lungs. The other clearance mechanism is provided by the <a href="/wiki/Cough_reflex" title="Cough reflex">cough reflex</a>.<sup id="cite_ref-Weinberger_2-0" class="reference"><a href="#cite_note-Weinberger-2"><span class="cite-bracket">[</span>2<span class="cite-bracket">]</span></a></sup> Mucociliary clearance has a major role in <a href="/wiki/Pulmonary_hygiene" title="Pulmonary hygiene">pulmonary hygiene</a>. </p><p>MCC effectiveness relies on the correct properties of the <a href="/wiki/Airway_surface_liquid" class="mw-redirect" title="Airway surface liquid">airway surface liquid</a> produced, both of the <a href="/wiki/Mucus#Respiratory_system" title="Mucus">periciliary sol layer</a> and the overlying <a href="/wiki/Mucus#Respiratory_system" title="Mucus">mucus gel layer</a>, and of the number and quality of the <a href="/wiki/Cilium" title="Cilium">cilia</a> present in the <a href="/wiki/Respiratory_epithelium" title="Respiratory epithelium">lining of the airways</a>.<sup id="cite_ref-Widdicombe_3-0" class="reference"><a href="#cite_note-Widdicombe-3"><span class="cite-bracket">[</span>3<span class="cite-bracket">]</span></a></sup> An important factor is the rate of <a href="/wiki/Mucin" title="Mucin">mucin</a> secretion. The <a href="/wiki/Ion_channel" title="Ion channel">ion channels</a> <a href="/wiki/CFTR" class="mw-redirect" title="CFTR">CFTR</a> and <a href="/wiki/ENaC" class="mw-redirect" title="ENaC">ENaC</a> work together to maintain the necessary hydration of the airway surface liquid.<sup id="cite_ref-4" class="reference"><a href="#cite_note-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> </p><p>Any disturbance in the closely regulated functioning of the cilia can cause a disease. Disturbances in the structural formation of the cilia can cause a number of <a href="/wiki/Ciliopathy" title="Ciliopathy">ciliopathies</a>, notably <a href="/wiki/Primary_ciliary_dyskinesia" title="Primary ciliary dyskinesia">primary ciliary dyskinesia</a>.<sup id="cite_ref-Horani_5-0" class="reference"><a href="#cite_note-Horani-5"><span class="cite-bracket">[</span>5<span class="cite-bracket">]</span></a></sup> <a href="/wiki/Tobacco_smoking" title="Tobacco smoking">Cigarette smoke exposure</a> can cause shortening of the cilia.<sup id="cite_ref-6" class="reference"><a href="#cite_note-6"><span class="cite-bracket">[</span>6<span class="cite-bracket">]</span></a></sup> </p> <meta property="mw:PageProp/toc" /> <div class="mw-heading mw-heading2"><h2 id="Function">Function</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=1" title="Edit section: Function"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>In the upper part of the respiratory tract, the <a href="/wiki/Nasal_hair" title="Nasal hair">nasal hair</a> in the <a href="/wiki/Nostril" title="Nostril">nostrils</a> traps large particles, and the <a href="/wiki/Sneeze" title="Sneeze">sneeze reflex</a> may also be triggered to expel them. The <a href="/wiki/Nasal_mucosa" title="Nasal mucosa">nasal mucosa</a> also traps particles preventing their entry further into the tract. In the rest of the respiratory tract, particles of different sizes become deposited along different parts of the airways. Larger particles are trapped higher up in the larger <a href="/wiki/Bronchus" title="Bronchus">bronchi</a>. As the airways become narrower only smaller particles can pass. The branchings of the airways cause turbulence in the airflow at all of their junctions where particles can then be deposited and they never reach the <a href="/wiki/Pulmonary_alveolus" title="Pulmonary alveolus">alveoli</a>. Only very small pathogens are able to gain entry to the alveoli. Mucociliary clearance functions to remove these particulates and also to trap and remove pathogens from the airways, in order to protect the delicate lung parenchyma, and also to provide protection and moisture to the airways.<sup id="cite_ref-Weinberger_2-1" class="reference"><a href="#cite_note-Weinberger-2"><span class="cite-bracket">[</span>2<span class="cite-bracket">]</span></a></sup> </p><p>Mucociliary clearance also takes part in <b>pulmonary elimination</b>, which with <a href="/wiki/Exhalation" title="Exhalation">exhalation</a> removes substances discharged from the <a href="/wiki/Pulmonary_capillaries" class="mw-redirect" title="Pulmonary capillaries">pulmonary capillaries</a> into the alveolar space.<sup id="cite_ref-MEsH_7-0" class="reference"><a href="#cite_note-MEsH-7"><span class="cite-bracket">[</span>7<span class="cite-bracket">]</span></a></sup> </p> <figure class="mw-default-size" typeof="mw:File/Thumb"><a href="/wiki/File:Bronchiolar_epithelium_3_-_SEM.jpg" class="mw-file-description"><img src="//upload.wikimedia.org/wikipedia/commons/thumb/3/39/Bronchiolar_epithelium_3_-_SEM.jpg/220px-Bronchiolar_epithelium_3_-_SEM.jpg" decoding="async" width="220" height="225" class="mw-file-element" srcset="//upload.wikimedia.org/wikipedia/commons/thumb/3/39/Bronchiolar_epithelium_3_-_SEM.jpg/330px-Bronchiolar_epithelium_3_-_SEM.jpg 1.5x, //upload.wikimedia.org/wikipedia/commons/thumb/3/39/Bronchiolar_epithelium_3_-_SEM.jpg/440px-Bronchiolar_epithelium_3_-_SEM.jpg 2x" data-file-width="1024" data-file-height="1049" /></a><figcaption><a href="/wiki/Scanning_electron_microscope" title="Scanning electron microscope">Scanning electron micrograph</a> of the cilia projecting from respiratory epithelium in the trachea involved in mucociliary clearance.</figcaption></figure> <div class="mw-heading mw-heading3"><h3 id="Components">Components</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=2" title="Edit section: Components"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>In the <a href="/wiki/Respiratory_tract" title="Respiratory tract">respiratory tract</a>, from the <a href="/wiki/Trachea" title="Trachea">trachea</a> to the <a href="/wiki/Terminal_bronchiole" class="mw-redirect" title="Terminal bronchiole">terminal bronchioles</a>, the lining is of <a href="/wiki/Respiratory_epithelium" title="Respiratory epithelium">respiratory epithelium</a> that is <a href="/wiki/Cilium" title="Cilium">ciliated</a>.<sup id="cite_ref-Hall_8-0" class="reference"><a href="#cite_note-Hall-8"><span class="cite-bracket">[</span>8<span class="cite-bracket">]</span></a></sup> The <a href="/wiki/Cilium#Motile_cilia" title="Cilium">cilia</a> are hair-like, <a href="/wiki/Microtubule" title="Microtubule">microtubular-based</a> structures on the <a href="/wiki/Lumen_(anatomy)" title="Lumen (anatomy)">luminal</a> surface of the <a href="/wiki/Epithelium" title="Epithelium">epithelium</a>. On each epithelial cell there are around 200 cilia that beat constantly at a rate of between 10 and 20 times per second. </p><p>The <a href="/wiki/Cilium#Motile_cilia" title="Cilium">cilia</a> are surrounded by a <a href="/wiki/Mucus#Respiratory_system" title="Mucus">periciliary liquid layer</a> (PCL), a <i>sol</i> layer that is overlain with the <i>gel</i> layer of <a href="/wiki/Mucus" title="Mucus">mucus</a>.<sup id="cite_ref-Derichs_9-0" class="reference"><a href="#cite_note-Derichs-9"><span class="cite-bracket">[</span>9<span class="cite-bracket">]</span></a></sup> These two components make up the <a href="/wiki/Epithelial_lining_fluid" class="mw-redirect" title="Epithelial lining fluid">epithelial lining fluid</a> (ELF), also known as the <a href="/wiki/Mucus" title="Mucus">airway surface liquid</a> (ASL), the composition of which is tightly regulated. The <a href="/wiki/Ion_channel" title="Ion channel">ion channels</a> <a href="/wiki/CFTR" class="mw-redirect" title="CFTR">CFTR</a>, and <a href="/wiki/ENaC" class="mw-redirect" title="ENaC">ENaC</a> work together to maintain the necessary hydration of the airway surface liquid.<sup id="cite_ref-10" class="reference"><a href="#cite_note-10"><span class="cite-bracket">[</span>10<span class="cite-bracket">]</span></a></sup> An important factor is the rate of <a href="/wiki/Mucin" title="Mucin">mucin</a> secretion. The mucus helps maintain epithelial moisture and traps <a href="/wiki/Particulates" title="Particulates">particulate material</a> and <a href="/wiki/Pathogen" title="Pathogen">pathogens</a> moving through the airway, and its composition determines how well mucociliary clearance works.<sup id="cite_ref-11" class="reference"><a href="#cite_note-11"><span class="cite-bracket">[</span>11<span class="cite-bracket">]</span></a></sup><sup id="cite_ref-Lewis_12-0" class="reference"><a href="#cite_note-Lewis-12"><span class="cite-bracket">[</span>12<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading3"><h3 id="Mechanism">Mechanism</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=3" title="Edit section: Mechanism"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <style data-mw-deduplicate="TemplateStyles:r1236090951">.mw-parser-output .hatnote{font-style:italic}.mw-parser-output div.hatnote{padding-left:1.6em;margin-bottom:0.5em}.mw-parser-output .hatnote i{font-style:normal}.mw-parser-output .hatnote+link+.hatnote{margin-top:-0.5em}@media print{body.ns-0 .mw-parser-output .hatnote{display:none!important}}</style><div role="note" class="hatnote navigation-not-searchable">Further information: <a href="/wiki/Intraflagellar_transport" title="Intraflagellar transport">Intraflagellar transport</a></div> <p>Within the thin periciliary liquid layer the cilia beat in a coordinated fashion directed to the <a href="/wiki/Pharynx" title="Pharynx">pharynx</a> where the transported mucus is either swallowed or coughed up. This movement towards the pharynx is either upward from the lower respiratory tract or downwards from the nasal structures clearing the mucus that is constantly produced.<sup id="cite_ref-Hall_8-1" class="reference"><a href="#cite_note-Hall-8"><span class="cite-bracket">[</span>8<span class="cite-bracket">]</span></a></sup> </p><p>Each cilium is about 7 <a href="/wiki/Micrometre" title="Micrometre">μm</a> in length,<sup id="cite_ref-Fahy_13-0" class="reference"><a href="#cite_note-Fahy-13"><span class="cite-bracket">[</span>13<span class="cite-bracket">]</span></a></sup> and is fixed at its base. Its beat has two parts: the power stroke, or effector stroke, and the recovery stroke.<sup id="cite_ref-Xu_14-0" class="reference"><a href="#cite_note-Xu-14"><span class="cite-bracket">[</span>14<span class="cite-bracket">]</span></a></sup><sup id="cite_ref-Wan2_15-0" class="reference"><a href="#cite_note-Wan2-15"><span class="cite-bracket">[</span>15<span class="cite-bracket">]</span></a></sup> The movement of the cilia takes place in the periciliary liquid which is a little shorter in depth than the height of an extended cilium. This allows the cilia to penetrate the mucous layer during its full extension in the effector stroke, and to propel the mucus directionally, away from the cell surface.<sup id="cite_ref-Xu_14-1" class="reference"><a href="#cite_note-Xu-14"><span class="cite-bracket">[</span>14<span class="cite-bracket">]</span></a></sup><sup id="cite_ref-Lewin_16-0" class="reference"><a href="#cite_note-Lewin-16"><span class="cite-bracket">[</span>16<span class="cite-bracket">]</span></a></sup> In the recovery stroke the cilium bends from one end to the other bringing it back to the starting point for the next power stroke.<sup id="cite_ref-Lewin_16-1" class="reference"><a href="#cite_note-Lewin-16"><span class="cite-bracket">[</span>16<span class="cite-bracket">]</span></a></sup> The returning cilia bend to immerse completely in the PCL which has the effect of reducing a reverse movement of mucus.<sup id="cite_ref-Xu_14-2" class="reference"><a href="#cite_note-Xu-14"><span class="cite-bracket">[</span>14<span class="cite-bracket">]</span></a></sup> </p> <figure class="mw-default-size" typeof="mw:File/Thumb"><a href="/wiki/File:Metachronal.svg" class="mw-file-description"><img src="//upload.wikimedia.org/wikipedia/commons/thumb/2/2f/Metachronal.svg/220px-Metachronal.svg.png" decoding="async" width="220" height="44" class="mw-file-element" srcset="//upload.wikimedia.org/wikipedia/commons/thumb/2/2f/Metachronal.svg/330px-Metachronal.svg.png 1.5x, //upload.wikimedia.org/wikipedia/commons/thumb/2/2f/Metachronal.svg/440px-Metachronal.svg.png 2x" data-file-width="1000" data-file-height="200" /></a><figcaption>Cilia movement in a <a href="/wiki/Metachronal_rhythm" title="Metachronal rhythm">metachronal wave.</a></figcaption></figure> <p>The coordinated movement of the cilia on all the cells is carried out in a fashion that is not clear. This produces wave-like motions that in the trachea, move at a speed of between 6 and 20 mm per minute.<sup id="cite_ref-Weinberger_2-2" class="reference"><a href="#cite_note-Weinberger-2"><span class="cite-bracket">[</span>2<span class="cite-bracket">]</span></a></sup> The wave produced is a <a href="/wiki/Metachronal_rhythm" title="Metachronal rhythm">metachronal wave</a> that moves the mucus.<sup id="cite_ref-Horani_5-1" class="reference"><a href="#cite_note-Horani-5"><span class="cite-bracket">[</span>5<span class="cite-bracket">]</span></a></sup> Many <a href="/wiki/Mathematical_model" title="Mathematical model">mathematical models</a> have been developed in order to study the mechanisms of ciliary beating. These include models to understand the generation and rhythm of the metachronal wave, and the generation of the force in the effective stroke of the cilium.<sup id="cite_ref-Xu_14-3" class="reference"><a href="#cite_note-Xu-14"><span class="cite-bracket">[</span>14<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading2"><h2 id="Clinical_significance">Clinical significance</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=4" title="Edit section: Clinical significance"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <figure class="mw-default-size" typeof="mw:File/Thumb"><a href="/wiki/File:Respiratory_Tract.jpg" class="mw-file-description"><img src="//upload.wikimedia.org/wikipedia/commons/thumb/f/ff/Respiratory_Tract.jpg/220px-Respiratory_Tract.jpg" decoding="async" width="220" height="124" class="mw-file-element" srcset="//upload.wikimedia.org/wikipedia/commons/thumb/f/ff/Respiratory_Tract.jpg/330px-Respiratory_Tract.jpg 1.5x, //upload.wikimedia.org/wikipedia/commons/thumb/f/ff/Respiratory_Tract.jpg/440px-Respiratory_Tract.jpg 2x" data-file-width="1920" data-file-height="1080" /></a><figcaption>Accumulated mucus in the airways resulting from impaired mucociliary clearance, that may involve mucus hypersecretion.</figcaption></figure> <p>Effective mucociliary clearance depends on a number of factors including the numbers of cilia, and their structure particularly their height, and the quality of the mucus produced that needs to be maintained at a correct <a href="/wiki/Humidity" title="Humidity">humidity</a>, temperature, and <a href="/wiki/PH" title="PH">acidity</a>. </p><p>The cilia need to be able to move freely in the periciliary liquid layer and when this is impaired through damage to the cilia or by imbalances in the moisture or <a href="/wiki/PH" title="PH">pH</a> of the PCL, the mucus is unable to be cleared properly from the airways. <a href="/wiki/Cystic_fibrosis" title="Cystic fibrosis">Cystic fibrosis</a> is a consequence of imbalances in the PCL.<sup id="cite_ref-Derichs_9-1" class="reference"><a href="#cite_note-Derichs-9"><span class="cite-bracket">[</span>9<span class="cite-bracket">]</span></a></sup> Accumulated mucus, apart from causing varying degrees of airflow obstruction, makes a breeding ground for bacteria that cause many respiratory infections that can <a href="/wiki/Exacerbation" title="Exacerbation">seriously worsen</a> existing lung disorders. <a href="/wiki/Obstructive_lung_disease" title="Obstructive lung disease">Obstructive lung diseases</a> often result from impaired mucociliary clearance that can be associated with <a href="/wiki/Mucus" title="Mucus">mucus hypersecretion</a> and these are sometimes referred to as <i>mucoobstructive lung diseases</i>.<sup id="cite_ref-Lewis_12-1" class="reference"><a href="#cite_note-Lewis-12"><span class="cite-bracket">[</span>12<span class="cite-bracket">]</span></a></sup> Studies have shown that the dehydration of airway surface liquid is enough to produce mucus obstruction even when there is no evidence of mucus hypersecretion.<sup id="cite_ref-17" class="reference"><a href="#cite_note-17"><span class="cite-bracket">[</span>17<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading3"><h3 id="Humidity">Humidity</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=5" title="Edit section: Humidity"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>High <a href="/wiki/Humidity" title="Humidity">humidity</a> enhances mucociliary clearance. One study in dogs found that mucus transport was lower at an absolute humidity of 9 g water/m<sup>3</sup> than at 30 g water/m<sup>3</sup>.<sup id="cite_ref-MRM_18-0" class="reference"><a href="#cite_note-MRM-18"><span class="cite-bracket">[</span>18<span class="cite-bracket">]</span></a></sup> Two methods of supporting this, particularly in <a href="/wiki/Mechanical_ventilation" title="Mechanical ventilation">mechanical ventilation</a>, are provided by active and passive <a href="/wiki/Respiratory_gas_humidification" title="Respiratory gas humidification">respiratory gas humidifiers</a>. </p> <div class="mw-heading mw-heading2"><h2 id="See_also">See also</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=6" title="Edit section: See also"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <ul><li><a href="/wiki/Airway_clearance_therapy" title="Airway clearance therapy">Airway clearance therapy</a></li></ul> <div class="mw-heading mw-heading2"><h2 id="References">References</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Mucociliary_clearance&action=edit&section=7" title="Edit section: References"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <style data-mw-deduplicate="TemplateStyles:r1239543626">.mw-parser-output .reflist{margin-bottom:0.5em;list-style-type:decimal}@media screen{.mw-parser-output .reflist{font-size:90%}}.mw-parser-output .reflist .references{font-size:100%;margin-bottom:0;list-style-type:inherit}.mw-parser-output .reflist-columns-2{column-width:30em}.mw-parser-output .reflist-columns-3{column-width:25em}.mw-parser-output .reflist-columns{margin-top:0.3em}.mw-parser-output .reflist-columns ol{margin-top:0}.mw-parser-output .reflist-columns li{page-break-inside:avoid;break-inside:avoid-column}.mw-parser-output .reflist-upper-alpha{list-style-type:upper-alpha}.mw-parser-output .reflist-upper-roman{list-style-type:upper-roman}.mw-parser-output .reflist-lower-alpha{list-style-type:lower-alpha}.mw-parser-output .reflist-lower-greek{list-style-type:lower-greek}.mw-parser-output .reflist-lower-roman{list-style-type:lower-roman}</style><div class="reflist"> <div class="mw-references-wrap mw-references-columns"><ol class="references"> <li id="cite_note-1"><span class="mw-cite-backlink"><b><a href="#cite_ref-1">^</a></b></span> <span class="reference-text"><style data-mw-deduplicate="TemplateStyles:r1238218222">.mw-parser-output cite.citation{font-style:inherit;word-wrap:break-word}.mw-parser-output .citation q{quotes:"\"""\"""'""'"}.mw-parser-output .citation:target{background-color:rgba(0,127,255,0.133)}.mw-parser-output .id-lock-free.id-lock-free a{background:url("//upload.wikimedia.org/wikipedia/commons/6/65/Lock-green.svg")right 0.1em center/9px no-repeat}.mw-parser-output .id-lock-limited.id-lock-limited a,.mw-parser-output .id-lock-registration.id-lock-registration a{background:url("//upload.wikimedia.org/wikipedia/commons/d/d6/Lock-gray-alt-2.svg")right 0.1em center/9px no-repeat}.mw-parser-output .id-lock-subscription.id-lock-subscription a{background:url("//upload.wikimedia.org/wikipedia/commons/a/aa/Lock-red-alt-2.svg")right 0.1em center/9px no-repeat}.mw-parser-output .cs1-ws-icon a{background:url("//upload.wikimedia.org/wikipedia/commons/4/4c/Wikisource-logo.svg")right 0.1em center/12px no-repeat}body:not(.skin-timeless):not(.skin-minerva) .mw-parser-output .id-lock-free a,body:not(.skin-timeless):not(.skin-minerva) .mw-parser-output .id-lock-limited a,body:not(.skin-timeless):not(.skin-minerva) .mw-parser-output .id-lock-registration a,body:not(.skin-timeless):not(.skin-minerva) .mw-parser-output .id-lock-subscription a,body:not(.skin-timeless):not(.skin-minerva) .mw-parser-output .cs1-ws-icon a{background-size:contain;padding:0 1em 0 0}.mw-parser-output .cs1-code{color:inherit;background:inherit;border:none;padding:inherit}.mw-parser-output .cs1-hidden-error{display:none;color:var(--color-error,#d33)}.mw-parser-output .cs1-visible-error{color:var(--color-error,#d33)}.mw-parser-output .cs1-maint{display:none;color:#085;margin-left:0.3em}.mw-parser-output .cs1-kern-left{padding-left:0.2em}.mw-parser-output .cs1-kern-right{padding-right:0.2em}.mw-parser-output .citation .mw-selflink{font-weight:inherit}@media screen{.mw-parser-output .cs1-format{font-size:95%}html.skin-theme-clientpref-night .mw-parser-output .cs1-maint{color:#18911f}}@media screen and (prefers-color-scheme:dark){html.skin-theme-clientpref-os .mw-parser-output .cs1-maint{color:#18911f}}</style><cite id="CITEREFAntunesCohen2007" class="citation journal cs1">Antunes, MB; Cohen, NA (February 2007). 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