Imaging of cardiovascular risk in patients with Turner's syndrome
Identifieur interne : 007317 ( Ncbi/Merge ); précédent : 007316; suivant : 007318Imaging of cardiovascular risk in patients with Turner's syndrome
Auteurs : A. Marin [Royaume-Uni] ; J. R. Weir-Mccall [Royaume-Uni] ; D. J. Webb [Royaume-Uni] ; E. J. R. Van Beek [Royaume-Uni] ; S. Mirsadraee [Royaume-Uni]Source :
- Clinical Radiology [ 0009-9260 ] ; 2015.
Abstract
Turner's syndrome is a disorder defined by an absent or structurally abnormal second X chromosome and affects around 1 in 2000 newborn females. The standardised mortality ratio in Turner's syndrome is around three-times higher than in the general female population, mainly as a result of cardiovascular disorders. Most striking is the early age at which Turner's syndrome patients develop the life-threatening complications of cardiovascular disorders compared to the general population. The cardiovascular risk stratification in Turner's syndrome is challenging and imaging is not systematically used. The aim of this article is to review cardiovascular risks in this group of patients and discuss a systematic imaging approach for early identification of cardiovascular disorders in these patients.
Url:
DOI: 10.1016/j.crad.2015.03.009
PubMed: 25917542
PubMed Central: 4509713
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<front><div type="abstract" xml:lang="en"><p>Turner's syndrome is a disorder defined by an absent or structurally abnormal second X chromosome and affects around 1 in 2000 newborn females. The standardised mortality ratio in Turner's syndrome is around three-times higher than in the general female population, mainly as a result of cardiovascular disorders. Most striking is the early age at which Turner's syndrome patients develop the life-threatening complications of cardiovascular disorders compared to the general population. The cardiovascular risk stratification in Turner's syndrome is challenging and imaging is not systematically used. The aim of this article is to review cardiovascular risks in this group of patients and discuss a systematic imaging approach for early identification of cardiovascular disorders in these patients.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Clin Radiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Clin Radiol</journal-id>
<journal-title-group><journal-title>Clinical Radiology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0009-9260</issn>
<issn pub-type="epub">1365-229X</issn>
<publisher><publisher-name>Blackwell Scientific Publications Ltd</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25917542</article-id>
<article-id pub-id-type="pmc">4509713</article-id>
<article-id pub-id-type="publisher-id">S0009-9260(15)00105-1</article-id>
<article-id pub-id-type="doi">10.1016/j.crad.2015.03.009</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Imaging of cardiovascular risk in patients with Turner's syndrome</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Marin</surname>
<given-names>A.</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Weir-McCall</surname>
<given-names>J.R.</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Webb</surname>
<given-names>D.J.</given-names>
</name>
<xref rid="aff3" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author"><name><surname>van Beek</surname>
<given-names>E.J.R.</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mirsadraee</surname>
<given-names>S.</given-names>
</name>
<email>smirsadr@staffmail.ed.ac.uk</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>a</label>
Clinical Research Imaging Centre, Queen's Medical Research Institute, University of Edinburgh, Edinburgh EH16 4TJ, UK</aff>
<aff id="aff2"><label>b</label>
Division of Cardiovascular and Diabetes Medicine, Ninewells Hospital & Medical School, Dundee DD1 9SY, UK</aff>
<aff id="aff3"><label>c</label>
Queen's Medical Research Institute, University of Edinburgh/BHF Centre for Cardiovascular Science, Edinburgh EH16 4TJ, UK</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Guarantor and correspondent: S. Mirsadraee, Clinical Research Imaging Centre, Queen's Medical Research Institute, University of Edinburgh, 47 Little France Crescent, Edinburgh EH16 4TJ, UK. Tel.: +44 131 2427768; fax: +44 131 2427773. <email>smirsadr@staffmail.ed.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>1</day>
<month>8</month>
<year>2015</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>8</month>
<year>2015</year>
</pub-date>
<volume>70</volume>
<issue>8</issue>
<fpage>803</fpage>
<lpage>814</lpage>
<history><date date-type="received"><day>17</day>
<month>12</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>17</day>
<month>2</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>19</day>
<month>3</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>© 2015 The Authors</copyright-statement>
<copyright-year>2015</copyright-year>
<license license-type="CC BY" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).</license-p>
</license>
</permissions>
<abstract><p>Turner's syndrome is a disorder defined by an absent or structurally abnormal second X chromosome and affects around 1 in 2000 newborn females. The standardised mortality ratio in Turner's syndrome is around three-times higher than in the general female population, mainly as a result of cardiovascular disorders. Most striking is the early age at which Turner's syndrome patients develop the life-threatening complications of cardiovascular disorders compared to the general population. The cardiovascular risk stratification in Turner's syndrome is challenging and imaging is not systematically used. The aim of this article is to review cardiovascular risks in this group of patients and discuss a systematic imaging approach for early identification of cardiovascular disorders in these patients.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Total and cause-specific SMR in Turner's syndrome by main diagnostic groups, from the Denmark<xref rid="bib2" ref-type="bibr"><sup>2</sup>
</xref>
and Great Britain<xref rid="bib3" ref-type="bibr"><sup>3</sup>
</xref>
cohort studies data. SMR is the ratio of deaths in the study population compared with the number expected from rates in the general population. The Danish study used the ICD-10, while the study from Great Britain used ICD-9 for the classification of diagnostic groups. Some cause-specific diagnostic subcategories (e.g., diseases of musculoskeletal system, aortic valve disease, cardiovascular congenital anomalies and aortic aneurysm) were not separately included in the Danish cohort study data. The high congenital anomalies SMR in Danish cohort is likely attributable to malformations of the heart and great arterial vessels.</p>
</caption>
<graphic xlink:href="gr1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Systolic cine MRI of the BAV in two patients with TS. (a) Demonstrates a R-L BAV (arrow) and (b) demonstrates a R-L BAV (arrow) with raphe (arrowhead).</p>
</caption>
<graphic xlink:href="gr2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Systolic bSSFP cine MRI of the aortic valve (a), the aortic root (b) and ascending aorta (c,d) in a 45-year-old TS patient with mild aortic stenosis and aortic regurgitation on transthoracic echocardiography, which was unable to assess the aortic dimensions. (a) Atrioventricular view demonstrates a L-R BAV (arrow), and (b) the three-chamber view shows an asymmetric jet flow through the BAV (arrow). (c) Shows the aortic root and ascending aorta in sagittal oblique (diameter measurements white lines) and left bottom figure (white frame) in axial views at the level of the main pulmonary artery.</p>
</caption>
<graphic xlink:href="gr3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>An oblique coronal left ventricular outflow tract cine image (bSSFP) end diastolic frame of a 50-year-old patient with TS. Right top figure (white frame) shows a normal tricuspid aortic valve (white arrow) in this patient. Measurements of the annulus (A), sinus of Valsalva (SV), sinotubular junction (STJ), and ascending aorta (AA) were within the normal limits for an adult patient: 20, 27, 22, and 32mm, respectively. However, the calculated ASI was 2.28 cm/m<sup>2</sup>
(body surface area = 1.4m<sup>2</sup>
) indicating a higher risk of future growth and/or dissection.</p>
</caption>
<graphic xlink:href="gr4"></graphic>
</fig>
<fig id="fig5"><label>Figure 5</label>
<caption><p>Volume-rendered MR aortography in a TS patient with previous aortic dissection and the residual coarctation (white arrow) and aortic aneurysm of descending thoracic aorta (white arrowhead) following surgical repair.</p>
</caption>
<graphic xlink:href="gr5"></graphic>
</fig>
<fig id="fig6"><label>Figure 6</label>
<caption><p>Sagittal oblique cine SSFP image of a 55-year-old TS patient showing a high-riding aorta (white arrow), residual coarctation after surgical repair (white arrowhead), and dilatation of ascending aorta (white dashed arrow), with the ASI >2.5.</p>
</caption>
<graphic xlink:href="gr6"></graphic>
</fig>
<fig id="fig7"><label>Figure 7</label>
<caption><p>A summary of recommended cardiovascular system imaging in patients with TS. (The grey highlighted section is adapted with permission from Turtle et al.<xref rid="bib8" ref-type="bibr"><sup>8</sup>
</xref>
) (a) When aortic dissection and/or coarctation is clinically suspected. (b) When MRI is not available or contraindicated. (c) When second transthoracic echocardiography is non-contributable. (d) When MRI can be without general sedation.</p>
</caption>
<graphic xlink:href="gr7"></graphic>
</fig>
<table-wrap id="tbl1" position="float"><label>Table 1</label>
<caption><p>The imaging findings of the associated congenital anomalies and acquired diseases in Turner's syndrome.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th>System</th>
<th>Congenital anomaly or acquired disease</th>
<th>Frequency/risk</th>
<th>Occurs in combination with</th>
</tr>
</thead>
<tbody><tr><td rowspan="7">Cardiovascular</td>
<td>Bicuspid aortic valve</td>
<td>30%<xref rid="bib22" ref-type="bibr"><sup>22</sup>
</xref>
(versus 1–2% in general population)<xref rid="bib21 bib22" ref-type="bibr"><sup>21,22</sup>
</xref>
</td>
<td>Aortic coarctation, neck webbing<xref rid="bib17" ref-type="bibr"><sup>17</sup>
</xref>
</td>
</tr>
<tr><td>Aortic dilatation</td>
<td>32–42%<xref rid="bib15 bib39 bib40" ref-type="bibr"><sup>15,39,40</sup>
</xref>
</td>
<td>BAV, aortic coarctation, hypertension or independently</td>
</tr>
<tr><td>Aortic dissection</td>
<td>100-fold increased risk, 36 cases/100,000 patient years (versus 6/100,000 in general population)<xref rid="bib9" ref-type="bibr"><sup>9</sup>
</xref>
</td>
<td>BAV, aortic coarctation, hypertension</td>
</tr>
<tr><td>Aortic coarctation</td>
<td>10–12%<xref rid="bib12 bib69" ref-type="bibr"><sup>12,69</sup>
</xref>
</td>
<td>BAV, neck webbing<xref rid="bib17" ref-type="bibr"><sup>17</sup>
</xref>
</td>
</tr>
<tr><td>Elongated transverse arch</td>
<td>49%<xref rid="bib12" ref-type="bibr"><sup>12</sup>
</xref>
</td>
<td></td>
</tr>
<tr><td>Partial anomalous pulmonary venous return</td>
<td>13%<xref rid="bib57" ref-type="bibr"><sup>57</sup>
</xref>
</td>
<td></td>
</tr>
<tr><td>Ischaemic heart disease</td>
<td>50%, appearing 6–13 years earlier than expected<xref rid="bib20" ref-type="bibr"><sup>20</sup>
</xref>
</td>
<td>Arterial hypertension, hyperlipidaemia</td>
</tr>
<tr><td rowspan="8">Skeletal</td>
<td>Osteoporosis</td>
<td>10–50%<xref rid="bib70 bib71 bib72" ref-type="bibr"><sup>70–72</sup>
</xref>
</td>
<td>Prolonged hypogonadism</td>
</tr>
<tr><td>Bone fractures</td>
<td>5–45%<xref rid="bib70 bib72" ref-type="bibr"><sup>70,72</sup>
</xref>
</td>
<td>Osteoporosis</td>
</tr>
<tr><td>Cervical vertebral hypoplasia</td>
<td></td>
<td></td>
</tr>
<tr><td>Scoliosis</td>
<td>5–10%<xref rid="bib73" ref-type="bibr"><sup>73</sup>
</xref>
</td>
<td>Growth hormone therapy</td>
</tr>
<tr><td>Cubitus valgus</td>
<td>Up to 50%</td>
<td></td>
</tr>
<tr><td>Genu valgum</td>
<td>60%<xref rid="bib74" ref-type="bibr"><sup>74</sup>
</xref>
</td>
<td></td>
</tr>
<tr><td>Short metacarpals and metatarsals</td>
<td></td>
<td></td>
</tr>
<tr><td>“Bayonet deformity” or Madelung's deformity</td>
<td></td>
<td></td>
</tr>
<tr><td>Renal</td>
<td>Horseshoe kidney, duplex systems, and long posteriorly rotated kidneys</td>
<td>33–38%<xref rid="bib75 bib76" ref-type="bibr"><sup>75,76</sup>
</xref>
</td>
<td></td>
</tr>
<tr><td>Reproductive</td>
<td>Gonadal dysgenesis</td>
<td>90% require hormone-replacement therapy<xref rid="bib4" ref-type="bibr"><sup>4</sup>
</xref>
</td>
<td></td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="tbl2" position="float"><label>Table 2</label>
<caption><p>Summary of studies looking at MRI assessment of aortic dilatation and dissection in Turner's syndrome.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th>Study</th>
<th>No</th>
<th>Sequence</th>
<th>Measurements</th>
<th>Findings</th>
</tr>
</thead>
<tbody><tr><td colspan="5">Aortic dilatation</td>
</tr>
<tr><td>Dawson-Falk 1992<xref rid="bib77" ref-type="bibr"><sup>77</sup>
</xref>
</td>
<td>40</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Axial stack through aorta with diameter measured on slice with most dilated aorta</td>
<td>Aortic dilation in 12.5% (indexed diameter >95th CI based on CT values). 80% of these were only seen on MRI</td>
</tr>
<tr><td>Castro 2002<xref rid="bib78" ref-type="bibr"><sup>78</sup>
</xref>
</td>
<td>15</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Axial stack through aorta with diameter measured 1 cm above aorta root</td>
<td>Ascending aortic dilation in 40% (indexed diameter >95th CI based on CT values); 26.7% had AD:DD >1.5</td>
</tr>
<tr><td>Ostberg 2004<xref rid="bib39" ref-type="bibr"><sup>39</sup>
</xref>
</td>
<td>115</td>
<td>No details</td>
<td>Ascending and descending aorta at level of right pulmonary artery</td>
<td>Ascending aorta dilated in 33% using MRI criteria (AD:DD >1.5), but only 7% met both MRI and echocardiography criteria for dilatation. Dilated root associated with age and BAV</td>
</tr>
<tr><td>Chalard 2005<xref rid="bib65" ref-type="bibr"><sup>65</sup>
</xref>
</td>
<td>21</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Two axial slices producing four measurements</td>
<td>19% (<italic>n</italic>
= 5) had ascending aortic dilatation (not defined)</td>
</tr>
<tr><td>Ilyas 2006<xref rid="bib79" ref-type="bibr"><sup>79</sup>
</xref>
</td>
<td>17</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Transverse plane (no further information provided)</td>
<td>Article focused on seven case series. <italic>n</italic>
= 1 with aortic dilatation, which developed and progressed during imaging follow-up</td>
</tr>
<tr><td>Bondy 2006<xref rid="bib80" ref-type="bibr"><sup>80</sup>
</xref>
</td>
<td>101</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Axial slice at level for ascending and descending aorta at level of RPA</td>
<td>Growth hormone has no effect on indexed aortic size</td>
</tr>
<tr><td>Matura 2007<xref rid="bib40" ref-type="bibr"><sup>40</sup>
</xref>
</td>
<td>166</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Ascending and descending aorta at level of RPA</td>
<td>32% have ASI >2. 9.5% have AD diameter >mean +2 SD of control population, 32% have ASI >2, 45% have AD:DD >1.5</td>
</tr>
<tr><td>Lanzarini 2007<xref rid="bib32" ref-type="bibr"><sup>32</sup>
</xref>
</td>
<td>59</td>
<td></td>
<td>Five levels within the thoracic aorta and one in the proximal abdominal aorta</td>
<td>Good correlation between echo and CMR in ascending aorta, however poorer correlation in rest of aorta.</td>
</tr>
<tr><td>Sachdev 2008<xref rid="bib22" ref-type="bibr"><sup>22</sup>
</xref>
</td>
<td>15</td>
<td>ECG-gated T1W “black blood” TSE sequence</td>
<td>Four locations in ascending aorta (annulus, sinus, STJ, ascending aorta)</td>
<td>Aortic root dilated (indexed diameter >mean +2 SD) in 25% of patients with BAV compared with 5% of TAV</td>
</tr>
<tr><td>Cleeman 2010<xref rid="bib81" ref-type="bibr"><sup>81</sup>
</xref>
</td>
<td>41</td>
<td>3D SSFP at diastole</td>
<td>Nine locations in thoracic aorta</td>
<td>No dilatation in mean aortic diameter, however aortic dilatation (indexed diameter >mean +2 SD of control group) was present in <italic>n</italic>
= 5 in at least one of the nine measured locations. Using AD:DD, dilation was present in 28% of TS and 32% of controls.</td>
</tr>
<tr><td>Hjerrild 2010<xref rid="bib41" ref-type="bibr"><sup>41</sup>
</xref>
<sup>,</sup>
<xref rid="tbl2fna" ref-type="table-fn">a</xref>
</td>
<td>102</td>
<td>3D SSFP at diastole</td>
<td>Eight locations in thoracic aorta</td>
<td>23% had aortic dilation (indexed diameter >mean +2 SD) in at least one location, with dilation in ≥2 locations in 14%. In the latter group, 85% had BAV. Aortic diameter correlated with age, sex, BP, and presence of CoA and BAV.</td>
</tr>
<tr><td>Mortensen 2010<xref rid="bib52" ref-type="bibr"><sup>52</sup>
</xref>
<sup>,</sup>
<xref rid="tbl2fna" ref-type="table-fn">a</xref>
</td>
<td>99</td>
<td>3D SSFP at diastole</td>
<td>Eight locations in thoracic aorta</td>
<td>TS have 6.7X RR of ascending aortic dilation compared to the general population. Ascending aorta dilation associated with BAV and aortic coarctation and 45X monosomy.</td>
</tr>
<tr><td>Kim 2011<xref rid="bib82" ref-type="bibr"><sup>82</sup>
</xref>
</td>
<td>51</td>
<td>MRA</td>
<td>Nine locations in thoracic aorta</td>
<td>Ascending aorta dilatation was common, with 30% with dilated aortic sinus (indexed diameter >mean +2 SD). 40.8% had AD:DD >1.5.</td>
</tr>
<tr><td>Mortensen 2011<xref rid="bib24" ref-type="bibr"><sup>24</sup>
</xref>
<sup>,</sup>
<xref rid="tbl2fna" ref-type="table-fn">a</xref>
</td>
<td>80</td>
<td>3D SSFP at diastole</td>
<td>Nine locations in thoracic aorta at baseline and 2 yrs follow-up</td>
<td>At a mean follow-up of 2.4 ± 0.4 yrs, increased dilatation was seen in the aortic sinus, sinotubular junction and mid-ascending aorta. Mean growth rate 0.1–0.4 mm/yr. BAV associated with more rapid growth rate than TAV (0.44 ± 0.57 versus 0.18 ± 0.61 mm/yr/m<sup>2</sup>
)</td>
</tr>
<tr><td>Mortensen 2013<xref rid="bib44" ref-type="bibr"><sup>44</sup>
</xref>
<sup>,</sup>
<xref rid="tbl2fna" ref-type="table-fn">a</xref>
</td>
<td>102</td>
<td>3D SSFP at diastole</td>
<td>Eight locations in thoracic aorta at baseline, 2 yrs and 5 yrs</td>
<td>Significant growth seen in ascending but not descending aorta. Growth rates varied from 0.20 ± 0.34 to 0.38 ± 0.46 mm/yr for the three most proximal ascending aorta measurements. Age, CoA, BAV were associated with an accelerated growth while diastolic BP and hypertensive treatment were associated with slower growth</td>
</tr>
<tr><td colspan="5">Aortic dissection</td>
</tr>
<tr><td>Study</td>
<td>No</td>
<td>Age</td>
<td>Measurements</td>
<td>Findings</td>
</tr>
<tr><td>Carlson 2007<xref rid="bib49" ref-type="bibr"><sup>49</sup>
</xref>
</td>
<td>2 (+85 literature review)</td>
<td>30.7 (4–64)</td>
<td>Echocardiography</td>
<td>15% had hypertension, 30% had congenital heart disease, 34% had both, 11% had no known risk factors. Assisted reproduction was present in 7/85, in this cohort there was an 86% mortality</td>
</tr>
<tr><td>Matura 2007<xref rid="bib40" ref-type="bibr"><sup>40</sup>
</xref>
</td>
<td>3</td>
<td>49.3 (44–47)</td>
<td>MRI with black blood axial sequence at level of right pulmonary artery</td>
<td>All had ASI >2.5. Dissection occurred in 25% with AD >3.5cm, 33% of those with ASI >2.5, and only 3% with AD:DD >1.5. Annualised rate of 618/100,000 woman yrs</td>
</tr>
<tr><td>Carlson 2012<xref rid="bib46" ref-type="bibr"><sup>46</sup>
</xref>
</td>
<td>20</td>
<td>31.5 (18–48)</td>
<td>Echocardiography in <italic>n</italic>
= 15</td>
<td>Twenty dissections in 22 yrs. Type A dissection in 85%, type B in 15%. Mean ASI was 2.7 ± 0.6 cm/m<sup>2</sup>
; 95% spontaneous dissections had a BAV, with 26% having an additional aortic pathology</td>
</tr>
<tr><td>Gravholt 2006<xref rid="bib9" ref-type="bibr"><sup>9</sup>
</xref>
<sup>,</sup>
<xref rid="tbl2fnb" ref-type="table-fn">b</xref>
</td>
<td>18</td>
<td>35 (18–61)</td>
<td>Echocardiography in <italic>n</italic>
= 10</td>
<td>Fourteen were 45X, 5 had BAV, and 5 had hypertension. Histology was available in 7 with 3 showing cystic medial necrosis. Estimated incidence of 36/100,000, compared with 6/100,000 in the general population (although the latter is not age matched)</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="tbl2fna"><label>a</label>
<p>Same centre with overlapping populations.</p>
</fn>
</table-wrap-foot>
<table-wrap-foot><fn id="tbl2fnb"><label>b</label>
<p>Included in Carlson literature review. Included separately as this is the only large-scale epidemiological review of dissection in TS.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Royaume-Uni</li>
</country>
<region><li>Écosse</li>
</region>
<settlement><li>Édimbourg</li>
</settlement>
<orgName><li>Université d'Édimbourg</li>
</orgName>
</list>
<tree><country name="Royaume-Uni"><region name="Écosse"><name sortKey="Marin, A" sort="Marin, A" uniqKey="Marin A" first="A." last="Marin">A. Marin</name>
</region>
<name sortKey="Mirsadraee, S" sort="Mirsadraee, S" uniqKey="Mirsadraee S" first="S." last="Mirsadraee">S. Mirsadraee</name>
<name sortKey="Van Beek, E J R" sort="Van Beek, E J R" uniqKey="Van Beek E" first="E. J. R." last="Van Beek">E. J. R. Van Beek</name>
<name sortKey="Webb, D J" sort="Webb, D J" uniqKey="Webb D" first="D. J." last="Webb">D. J. Webb</name>
<name sortKey="Weir Mccall, J R" sort="Weir Mccall, J R" uniqKey="Weir Mccall J" first="J. R." last="Weir-Mccall">J. R. Weir-Mccall</name>
</country>
</tree>
</affiliations>
</record>
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