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Causes of oocyte abnormalities subsection</span> </button> <ul id="toc-Causes_of_oocyte_abnormalities-sublist" class="vector-toc-list"> <li id="toc-Causes_of_premature_ovarian_insufficiency" class="vector-toc-list-item vector-toc-level-2"> <a class="vector-toc-link" href="#Causes_of_premature_ovarian_insufficiency"> <div class="vector-toc-text"> <span class="vector-toc-numb">1.1</span> <span>Causes of premature ovarian insufficiency</span> </div> </a> <ul id="toc-Causes_of_premature_ovarian_insufficiency-sublist" class="vector-toc-list"> </ul> </li> </ul> </li> <li id="toc-Oocyte_maturation_abnormalities_(OMAS)" class="vector-toc-list-item vector-toc-level-1 vector-toc-list-item-expanded"> <a class="vector-toc-link" href="#Oocyte_maturation_abnormalities_(OMAS)"> <div class="vector-toc-text"> <span class="vector-toc-numb">2</span> <span>Oocyte maturation abnormalities (OMAS)</span> </div> </a> <ul id="toc-Oocyte_maturation_abnormalities_(OMAS)-sublist" class="vector-toc-list"> </ul> </li> <li id="toc-Ageing_oocytes" class="vector-toc-list-item vector-toc-level-1 vector-toc-list-item-expanded"> <a class="vector-toc-link" href="#Ageing_oocytes"> <div class="vector-toc-text"> <span class="vector-toc-numb">3</span> <span>Ageing oocytes</span> </div> </a> <ul id="toc-Ageing_oocytes-sublist" class="vector-toc-list"> </ul> </li> <li id="toc-Mitochondria_abnormalities" class="vector-toc-list-item vector-toc-level-1 vector-toc-list-item-expanded"> <a class="vector-toc-link" href="#Mitochondria_abnormalities"> <div class="vector-toc-text"> <span class="vector-toc-numb">4</span> <span>Mitochondria abnormalities</span> </div> </a> <button aria-controls="toc-Mitochondria_abnormalities-sublist" class="cdx-button cdx-button--weight-quiet cdx-button--icon-only vector-toc-toggle"> <span class="vector-icon mw-ui-icon-wikimedia-expand"></span> <span>Toggle Mitochondria abnormalities subsection</span> </button> <ul id="toc-Mitochondria_abnormalities-sublist" class="vector-toc-list"> <li id="toc-Age" class="vector-toc-list-item vector-toc-level-2"> <a class="vector-toc-link" href="#Age"> <div class="vector-toc-text"> <span class="vector-toc-numb">4.1</span> <span>Age</span> </div> </a> <ul id="toc-Age-sublist" class="vector-toc-list"> </ul> </li> <li id="toc-Obesity" class="vector-toc-list-item vector-toc-level-2"> <a class="vector-toc-link" href="#Obesity"> <div class="vector-toc-text"> <span class="vector-toc-numb">4.2</span> <span>Obesity</span> </div> </a> <ul id="toc-Obesity-sublist" class="vector-toc-list"> </ul> </li> </ul> </li> <li id="toc-Nondisjunction" class="vector-toc-list-item vector-toc-level-1 vector-toc-list-item-expanded"> <a class="vector-toc-link" href="#Nondisjunction"> <div class="vector-toc-text"> <span class="vector-toc-numb">5</span> <span>Nondisjunction</span> </div> </a> <ul id="toc-Nondisjunction-sublist" class="vector-toc-list"> </ul> </li> <li id="toc-References" class="vector-toc-list-item vector-toc-level-1 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searchaux" style="display:none">Egg cell abnormalities</div> <p><a href="/wiki/Oocyte" title="Oocyte">Oocytes</a> are immature <a href="/wiki/Egg_cell" title="Egg cell">egg cells</a> that develop to maturity within a <a href="/wiki/Follicle_cell" class="mw-redirect" title="Follicle cell">follicle</a> in the <a href="/wiki/Ovary" title="Ovary">ovary</a>. <b>Oocyte abnormalities</b> can occur due to several factors, including <a href="/wiki/Primary_ovarian_insufficiency" title="Primary ovarian insufficiency">premature ovarian insufficiency (POI)</a>, other maturation abnormalities, maternal ageing, and <a href="/wiki/Mitochondrion" title="Mitochondrion">mitochondrial</a> abnormalities. </p> <meta property="mw:PageProp/toc" /> <div class="mw-heading mw-heading2"><h2 id="Causes_of_oocyte_abnormalities">Causes of oocyte abnormalities</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=1" title="Edit section: Causes of oocyte abnormalities"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Oocyte abnormalities can be caused by a variety of <a href="/wiki/Genetics" title="Genetics">genetic factors</a> affecting different stages in <a href="/wiki/Meiosis" title="Meiosis">meiosis</a>.<sup id="cite_ref-:4_1-0" class="reference"><a href="#cite_note-:4-1"><span class="cite-bracket">[</span>1<span class="cite-bracket">]</span></a></sup> Moreover, ageing is associated with oocyte abnormalities since higher maternal age is associated with oocytes with a reduced gene expression of <a href="/wiki/Spindle_checkpoint" title="Spindle checkpoint">spindle assembly checkpoints</a> which are important in maintaining stability in the genome. A high maternal age is associated with increased <a href="/wiki/Chromosome_segregation" title="Chromosome segregation">chromosome segregation</a> errors during meiosis as well, which leads to oocyte abnormalities.<sup id="cite_ref-:5_2-0" class="reference"><a href="#cite_note-:5-2"><span class="cite-bracket">[</span>2<span class="cite-bracket">]</span></a></sup> </p><p><a href="/wiki/Diet_(nutrition)" title="Diet (nutrition)">Diet</a> appears to also potentially have an effect on oocyte quality and a better diet seems to improve <a href="/wiki/Fertility" title="Fertility">fertility</a> in that aspect. Specifically, regular intake of oral <a href="/wiki/Antioxidant" title="Antioxidant">antioxidants</a> (mixture of vitamin C and E) was shown to reduce the negative effect of ageing on oocyte quantity and quality in female mice.<sup id="cite_ref-:5_2-1" class="reference"><a href="#cite_note-:5-2"><span class="cite-bracket">[</span>2<span class="cite-bracket">]</span></a></sup> </p><p><a href="/wiki/Chemotherapy" title="Chemotherapy">Chemotherapy</a> also has an impact on the ovary and subsequently on the oocyte and <a href="/wiki/Granulosa_cell" title="Granulosa cell">granulosa cells</a>.<sup id="cite_ref-3" class="reference"><a href="#cite_note-3"><span class="cite-bracket">[</span>3<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading3"><h3 id="Causes_of_premature_ovarian_insufficiency">Causes of premature ovarian insufficiency</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=2" title="Edit section: Causes of premature ovarian insufficiency"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Premature ovarian insufficiency (POI) is impairment of the ovaries and how they work before the age of 40 years. It can be caused by multiple factors, one being genetic. Genes and their influence determine the initial number of the primordial follicles, impact on the rate of <a href="/wiki/Follicular_atresia" title="Follicular atresia">follicular atresia</a>, and are impactful on the age of <a href="/wiki/Menopause" title="Menopause">menopause</a>. With the advent of more sophisticated <a href="/wiki/Genetic_screening" class="mw-redirect" title="Genetic screening">genetic screening technologies</a>, 20 to 25% of cases of POI appear to be of genetic origin. There are cases where the origin of the condition cannot be defined or explained, and these are called idiopathic causes. Another cause could be <a href="/wiki/Autoimmunity" title="Autoimmunity">autoimmunity</a>, as more than 20% of women with POI have autoimmune diseases associated with the condition, such as <a href="/wiki/Graves%27_disease" title="Graves' disease">Grave's</a> or <a href="/wiki/Hashimoto%27s_thyroiditis" title="Hashimoto's thyroiditis">Hashimoto's</a>. Infections, such as <a href="/wiki/Mumps" title="Mumps">mumps</a>, <a href="/wiki/Tuberculosis" title="Tuberculosis">tuberculosis</a> and <a href="/wiki/Malaria" title="Malaria">malaria</a> can also be causes of POI.<sup id="cite_ref-:4_1-1" class="reference"><a href="#cite_note-:4-1"><span class="cite-bracket">[</span>1<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading2"><h2 id="Oocyte_maturation_abnormalities_(OMAS)"><span id="Oocyte_maturation_abnormalities_.28OMAS.29"></span>Oocyte maturation abnormalities (OMAS)</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=3" title="Edit section: Oocyte maturation abnormalities (OMAS)"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Oocyte maturation abnormalities (OMAS) are repeatedly experienced in a small percentage of <a href="/wiki/Infertility" title="Infertility">infertile women</a>.<sup id="cite_ref-:0_4-0" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> These are problems with the maturation of oocytes; the step in oocyte development that occurs just before <a href="/wiki/Ovulation" title="Ovulation">ovulation</a> and successive <a href="/wiki/Fertilisation" title="Fertilisation">fertilisation</a>.<sup id="cite_ref-:1_5-0" class="reference"><a href="#cite_note-:1-5"><span class="cite-bracket">[</span>5<span class="cite-bracket">]</span></a></sup> </p><p>Oocytes must mature in order to reach reproductive potential.<sup id="cite_ref-:0_4-1" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> Until <a href="/wiki/Puberty" title="Puberty">puberty</a>, oocytes are kept in a dormant state in <a href="/wiki/Primordial_follicles" class="mw-redirect" title="Primordial follicles">primordial follicles</a>.<sup id="cite_ref-:0_4-2" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> At puberty the oocyte must exit its dormant stage and re-enter meiosis in order for ovulation to occur.<sup id="cite_ref-:1_5-1" class="reference"><a href="#cite_note-:1-5"><span class="cite-bracket">[</span>5<span class="cite-bracket">]</span></a></sup> </p><p>OMAS are usually diagnosed in women attempting <a href="/wiki/In_vitro_fertilisation" title="In vitro fertilisation">in vitro fertilisation (IVF)</a>, and include premature ovarian insufficiency (POI), degenerated and dysmorphic oocytes, <a href="/w/index.php?title=Empty_follicle_syndrome&action=edit&redlink=1" class="new" title="Empty follicle syndrome (page does not exist)">empty follicle syndrome (EFS)</a>, oocyte maturation arrest, and <a href="/wiki/Resistant_ovary_syndrome" class="mw-redirect" title="Resistant ovary syndrome">resistant ovary syndrome (ROS)</a>.<sup id="cite_ref-:0_4-3" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> </p> <ul><li>Degenerated and dysmorphic oocytes are not uncommon in <a href="/wiki/Assisted_reproductive_technology" title="Assisted reproductive technology">assisted reproduction</a>.<sup id="cite_ref-:0_4-4" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> Degenerated oocytes are classified as damaged oocytes or oocytes without a <a href="/wiki/Zona_pellucida" title="Zona pellucida">zona pellucida</a>.<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> Dysmorphic oocytes are oocytes with abnormal physical characteristics, for example multiple <a href="/wiki/Cell_nucleus" title="Cell nucleus">nuclei</a>.<sup id="cite_ref-7" class="reference"><a href="#cite_note-7"><span class="cite-bracket">[</span>7<span class="cite-bracket">]</span></a></sup></li></ul> <ul><li>EFS is a condition occurring when no oocytes are produced from the mature follicle after ovulation is induced in cycles of in vitro fertilisation (IVF).<sup id="cite_ref-8" class="reference"><a href="#cite_note-8"><span class="cite-bracket">[</span>8<span class="cite-bracket">]</span></a></sup></li></ul> <ul><li>Oocyte maturation arrest can be sub-classified into five different types of arrest, depending on the stage of maturation they are arrested at: germinal vesicle (GV) arrest, Meiosis I (MI) arrest, Meisos II (MII) arrest, GV and MI combined arrest, and mixed arrest.<sup id="cite_ref-:0_4-5" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup></li></ul> <ul><li>ROS is when the oocyte does not respond to normal hormone signals, and has increased levels of <a href="/wiki/Follicle-stimulating_hormone" title="Follicle-stimulating hormone">follicle stimulating hormone (FSH)</a> and <a href="/wiki/Luteinizing_hormone" title="Luteinizing hormone">luteinising hormone (LH)</a>.<sup id="cite_ref-:0_4-6" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup> Persevering immature oocytes are often observed in this condition.<sup id="cite_ref-:0_4-7" class="reference"><a href="#cite_note-:0-4"><span class="cite-bracket">[</span>4<span class="cite-bracket">]</span></a></sup></li></ul> <div class="mw-heading mw-heading2"><h2 id="Ageing_oocytes">Ageing oocytes</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=4" title="Edit section: Ageing oocytes"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Maternal age and its negative effects on oocytes plays a key role in the reduction of fertility in women over 35 years of age.<sup id="cite_ref-Mikwar_2020_9-0" class="reference"><a href="#cite_note-Mikwar_2020-9"><span class="cite-bracket">[</span>9<span class="cite-bracket">]</span></a></sup> Ageing predominantly affects oocytes during their arrest in the <a href="/wiki/Prophase" title="Prophase">prophase</a> of meiosis I – where genetic stability is often undermined.<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> </p><p>The principal oocyte abnormality associated with increased maternal age is <a href="/wiki/Aneuploidy" title="Aneuploidy">aneuploidy</a>, in which chromosome segregation errors result in oocytes having the wrong number of chromosomes.<sup id="cite_ref-Mikwar_2020_9-1" class="reference"><a href="#cite_note-Mikwar_2020-9"><span class="cite-bracket">[</span>9<span class="cite-bracket">]</span></a></sup> </p><p>Causes for these errors are not fully understood however, some proposed mechanisms include:<sup id="cite_ref-Baumann_2021_11-0" class="reference"><a href="#cite_note-Baumann_2021-11"><span class="cite-bracket">[</span>11<span class="cite-bracket">]</span></a></sup><sup id="cite_ref-12" class="reference"><a href="#cite_note-12"><span class="cite-bracket">[</span>12<span class="cite-bracket">]</span></a></sup> </p> <ul><li>Oxidative stress, the impact of which is due to aging’s connection with increased levels of <a href="/wiki/Reactive_oxygen_species" title="Reactive oxygen species">reactive oxygen species</a> (ROS). When left unchecked this can result in follicular atresia and reduction in both the number and quality of oocytes.<sup id="cite_ref-13" class="reference"><a href="#cite_note-13"><span class="cite-bracket">[</span>13<span class="cite-bracket">]</span></a></sup></li> <li>Spindle assembly checkpoint malfunction causing gene imbalances that often result in the fertilised oocyte produced being incapable of developing further.<sup id="cite_ref-14" class="reference"><a href="#cite_note-14"><span class="cite-bracket">[</span>14<span class="cite-bracket">]</span></a></sup></li> <li>Cohesion loss due to a decrease in REC8-cohesin complex, which would normally maintain the integrity of paired chromosomes (bivalents).<sup id="cite_ref-:1_5-2" class="reference"><a href="#cite_note-:1-5"><span class="cite-bracket">[</span>5<span class="cite-bracket">]</span></a></sup></li> <li>DNA damage (especially involving radiation or chemotherapy) which results in oocyte elimination if picked up by the body.<sup id="cite_ref-15" class="reference"><a href="#cite_note-15"><span class="cite-bracket">[</span>15<span class="cite-bracket">]</span></a></sup></li></ul> <div class="mw-heading mw-heading2"><h2 id="Mitochondria_abnormalities">Mitochondria abnormalities</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=5" title="Edit section: Mitochondria abnormalities"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Normal function of mitochondria is to generate energy through <a href="/wiki/Oxidative_phosphorylation" title="Oxidative phosphorylation">oxidative phosphorylation</a>. During oocyte maturation and fertilization mitochondria elongate, develop <a href="/wiki/Crista" title="Crista">cristae</a> and the matrix changes from a dense solution to a lighter matrix. Any abnormalities in this mitochondria development can lead to chromosomal segment disorders, oocyte maturation failures and arrested cell division.<sup id="cite_ref-:2_16-0" class="reference"><a href="#cite_note-:2-16"><span class="cite-bracket">[</span>16<span class="cite-bracket">]</span></a></sup> </p><p>After mitochondria has fully completed conformational changes, the mitochondria DNA copy number (mtDNA) increases rapidly to support the oocyte into the blastocyst stage. Therefore a higher mtDNA number is associated with better oocyte quality and potential of fertility.<sup id="cite_ref-:3_17-0" class="reference"><a href="#cite_note-:3-17"><span class="cite-bracket">[</span>17<span class="cite-bracket">]</span></a></sup> There are several factors that effect mitochondria quality. These are listed below: </p> <div class="mw-heading mw-heading3"><h3 id="Age">Age</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=6" title="Edit section: Age"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Mitochondria appear more swollen and present disrupted cristae with increased age. They have also been found to have lower mtDNA, increased <a href="/wiki/Reactive_oxygen_species" title="Reactive oxygen species">reactive oxidative species</a> and expression of Bax which upregulates <a href="/wiki/Apoptosis" title="Apoptosis">apoptosis</a> of follicles and early embryo arrest.<sup id="cite_ref-:2_16-1" class="reference"><a href="#cite_note-:2-16"><span class="cite-bracket">[</span>16<span class="cite-bracket">]</span></a></sup> </p> <div class="mw-heading mw-heading3"><h3 id="Obesity">Obesity</h3><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=7" title="Edit section: Obesity"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Causes delayed maturation of oocytes whereby mitochondria display fewer and disarrayed cristae. The intracellular matrix has a lower electron density and increased swelling.<sup id="cite_ref-:3_17-1" class="reference"><a href="#cite_note-:3-17"><span class="cite-bracket">[</span>17<span class="cite-bracket">]</span></a></sup> </p><p>Both of these factors lead to an increased chance of miscarriage due to failure to implant into the uterine lining. </p> <div class="mw-heading mw-heading2"><h2 id="Nondisjunction">Nondisjunction</h2><span class="mw-editsection"><span class="mw-editsection-bracket">[</span><a href="/w/index.php?title=Oocyte_abnormalities&action=edit&section=8" title="Edit section: Nondisjunction"><span>edit</span></a><span class="mw-editsection-bracket">]</span></span></div> <p>Normally oocytes stay arrested at prophase of meiosis I. A surge in <a href="/wiki/Luteinizing_hormone" title="Luteinizing hormone">luteinising hormone</a> triggers ovulation of the oocyte and triggers the resumption of meiosis. The germinal vesicle breaks down and spindles assemble as homologous chromosomes align the cell's equator for the first meiotic chromosome segregation. Here the oocyte splits where sister chromatids migrate to the same pole and the first polar body is formed.<sup id="cite_ref-18" class="reference"><a href="#cite_note-18"><span class="cite-bracket">[</span>18<span class="cite-bracket">]</span></a></sup> The oocyte now enters meiosis II and remains arrested in metaphase II until fertilization where sister chromatids will separate. </p><p>During this process at least one crossover per homologous pair is required for successful chromosome segregation. If this does not occur it can result in <a href="/wiki/Nondisjunction" title="Nondisjunction">nondisjunction</a> and aneuploidy.<sup id="cite_ref-19" class="reference"><a href="#cite_note-19"><span class="cite-bracket">[</span>19<span class="cite-bracket">]</span></a></sup> There are several factors that contribute towards failed crossovers including: </p> <ul><li>Lack of cohesion along the chromosome arms means the chiasmata cannot be secured properly.<sup id="cite_ref-:6_20-0" class="reference"><a href="#cite_note-:6-20"><span class="cite-bracket">[</span>20<span class="cite-bracket">]</span></a></sup></li> <li>Failed chiasmata maintenance. Crossovers that occur towards the end of the telomere can slide off the end of the homologous chromosomes leading to premature separation of the homologs causing defective chromosome configurations.<sup id="cite_ref-:6_20-1" class="reference"><a href="#cite_note-:6-20"><span class="cite-bracket">[</span>20<span class="cite-bracket">]</span></a></sup></li> <li>Missegregation of sister chromatids during Metaphase II.<sup id="cite_ref-:6_20-2" class="reference"><a href="#cite_note-:6-20"><span class="cite-bracket">[</span>20<span class="cite-bracket">]</span></a></sup></li> <li>Age dependent weakening of sister chromatid cohesion.<sup id="cite_ref-21" class="reference"><a href="#cite_note-21"><span class="cite-bracket">[</span>21<span class="cite-bracket">]</span></a></sup></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=Oocyte_abnormalities&action=edit&section=9" 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-:4-1"><span class="mw-cite-backlink">^ <a href="#cite_ref-:4_1-0"><sup><i><b>a</b></i></sup></a> <a href="#cite_ref-:4_1-1"><sup><i><b>b</b></i></sup></a></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 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