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Structure-function relationships in the feto-placental circulation from in silico interpretation of micro-CT vascular structures
•The placenta provides a crucial nutrient exchange surface between mother and fetus.•Delivered placentae exhibit a wide range of vascular branching properties.•Our image-to-model framework aims to relate vascular branching to resistance.•Macro-scale vascular heterogeneities may indicate risk of elev...
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Published in: | Journal of theoretical biology 2021-05, Vol.517, p.110630-110630, Article 110630 |
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container_title | Journal of theoretical biology |
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description | •The placenta provides a crucial nutrient exchange surface between mother and fetus.•Delivered placentae exhibit a wide range of vascular branching properties.•Our image-to-model framework aims to relate vascular branching to resistance.•Macro-scale vascular heterogeneities may indicate risk of elevated resistance.•Anastomoses between umbilical arteries mitigate impact of vascular heterogeneity.
A well-functioning placenta is critical for healthy fetal development, as the placenta brings fetal blood in close contact with nutrient rich maternal blood, enabling exchange of nutrients and waste between mother and fetus. The feto-placental circulation forms a complex branching structure, providing blood to fetal capillaries, which must receive sufficient blood flow to ensure effective exchange, but at a low enough pressure to prevent damage to placental circulatory structures. The branching structure of the feto-placental circulation is known to be altered in complications such as fetal growth restriction, and the presence of regions of vascular dysfunction (such as hypovascularity or thrombosis) are proposed to elevate risk of placental pathology. Here we present a methodology to combine micro-computed tomography and computational model-based analysis of the branching structure of the feto-placental circulation in ex vivo placentae from normal term pregnancies. We analyse how vascular structure relates to function in this key organ of pregnancy; demonstrating that there is a ‘resilience’ to placental vascular structure–function relationships. We find that placentae with variable chorionic vascular structures, both with and without a Hyrtl’s anastomosis between the umbilical arteries, and those with multiple regions of poorly vascularised tissue are able to function with a normal vascular resistance. Our models also predict that by progressively introducing local heterogeneity in placental vascular structure, large increases in feto-placental vascular resistances are induced. This suggests that localised heterogeneities in placental structure could potentially provide an indicator of increased risk of placental dysfunction. |
doi_str_mv | 10.1016/j.jtbi.2021.110630 |
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A well-functioning placenta is critical for healthy fetal development, as the placenta brings fetal blood in close contact with nutrient rich maternal blood, enabling exchange of nutrients and waste between mother and fetus. The feto-placental circulation forms a complex branching structure, providing blood to fetal capillaries, which must receive sufficient blood flow to ensure effective exchange, but at a low enough pressure to prevent damage to placental circulatory structures. The branching structure of the feto-placental circulation is known to be altered in complications such as fetal growth restriction, and the presence of regions of vascular dysfunction (such as hypovascularity or thrombosis) are proposed to elevate risk of placental pathology. Here we present a methodology to combine micro-computed tomography and computational model-based analysis of the branching structure of the feto-placental circulation in ex vivo placentae from normal term pregnancies. We analyse how vascular structure relates to function in this key organ of pregnancy; demonstrating that there is a ‘resilience’ to placental vascular structure–function relationships. We find that placentae with variable chorionic vascular structures, both with and without a Hyrtl’s anastomosis between the umbilical arteries, and those with multiple regions of poorly vascularised tissue are able to function with a normal vascular resistance. Our models also predict that by progressively introducing local heterogeneity in placental vascular structure, large increases in feto-placental vascular resistances are induced. This suggests that localised heterogeneities in placental structure could potentially provide an indicator of increased risk of placental dysfunction.</description><identifier>ISSN: 0022-5193</identifier><identifier>EISSN: 1095-8541</identifier><identifier>DOI: 10.1016/j.jtbi.2021.110630</identifier><identifier>PMID: 33607145</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Computational model ; Haemodynamics ; Micro-CT ; Placenta</subject><ispartof>Journal of theoretical biology, 2021-05, Vol.517, p.110630-110630, Article 110630</ispartof><rights>2021 Elsevier Ltd</rights><rights>Copyright © 2021 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-8921fb74384ea396616309bd49133d14179d8f90c52e06d470a6a87acd238fab3</citedby><cites>FETCH-LOGICAL-c455t-8921fb74384ea396616309bd49133d14179d8f90c52e06d470a6a87acd238fab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33607145$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Byrne, Monika</creatorcontrib><creatorcontrib>Aughwane, Rosalind</creatorcontrib><creatorcontrib>James, Joanna L</creatorcontrib><creatorcontrib>Hutchinson, J Ciaran</creatorcontrib><creatorcontrib>Arthurs, Owen J</creatorcontrib><creatorcontrib>Sebire, Neil J</creatorcontrib><creatorcontrib>Ourselin, Sebastien</creatorcontrib><creatorcontrib>David, Anna L</creatorcontrib><creatorcontrib>Melbourne, Andrew</creatorcontrib><creatorcontrib>Clark, Alys R</creatorcontrib><title>Structure-function relationships in the feto-placental circulation from in silico interpretation of micro-CT vascular structures</title><title>Journal of theoretical biology</title><addtitle>J Theor Biol</addtitle><description>•The placenta provides a crucial nutrient exchange surface between mother and fetus.•Delivered placentae exhibit a wide range of vascular branching properties.•Our image-to-model framework aims to relate vascular branching to resistance.•Macro-scale vascular heterogeneities may indicate risk of elevated resistance.•Anastomoses between umbilical arteries mitigate impact of vascular heterogeneity.
A well-functioning placenta is critical for healthy fetal development, as the placenta brings fetal blood in close contact with nutrient rich maternal blood, enabling exchange of nutrients and waste between mother and fetus. The feto-placental circulation forms a complex branching structure, providing blood to fetal capillaries, which must receive sufficient blood flow to ensure effective exchange, but at a low enough pressure to prevent damage to placental circulatory structures. The branching structure of the feto-placental circulation is known to be altered in complications such as fetal growth restriction, and the presence of regions of vascular dysfunction (such as hypovascularity or thrombosis) are proposed to elevate risk of placental pathology. Here we present a methodology to combine micro-computed tomography and computational model-based analysis of the branching structure of the feto-placental circulation in ex vivo placentae from normal term pregnancies. We analyse how vascular structure relates to function in this key organ of pregnancy; demonstrating that there is a ‘resilience’ to placental vascular structure–function relationships. We find that placentae with variable chorionic vascular structures, both with and without a Hyrtl’s anastomosis between the umbilical arteries, and those with multiple regions of poorly vascularised tissue are able to function with a normal vascular resistance. Our models also predict that by progressively introducing local heterogeneity in placental vascular structure, large increases in feto-placental vascular resistances are induced. This suggests that localised heterogeneities in placental structure could potentially provide an indicator of increased risk of placental dysfunction.</description><subject>Computational model</subject><subject>Haemodynamics</subject><subject>Micro-CT</subject><subject>Placenta</subject><issn>0022-5193</issn><issn>1095-8541</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kU1r3DAQhkVpabZJ_0APRcdevNWXZQtKoSz9gkAOTc5ClkddLbblSvJCb_3plXES2ktOGphn3plXL0JvKNlTQuX70_6UO79nhNE9pURy8gztKFF11daCPkc7Qhiraqr4BXqV0okQogSXL9EF55I0VNQ79OdHjovNS4TKLZPNPkw4wmDWIh39nLCfcD4CdpBDNQ_GwpTNgK2Pdtkw7GIYVyz5wdtQqgxxjpC3bnB49DaG6nCLzyatUxGnh63pCr1wZkjw-v69RHdfPt8evlXXN1-_Hz5dV1bUda5axajrGsFbAYYrKWmxq7peKMp5TwVtVN86RWzNgMheNMRI0zbG9oy3znT8En3cdOelG6FfbUQz6Dn60cTfOhiv_-9M_qh_hrNuJOWCtEXg3b1ADL8WSFmPPlkYBjNBWJJm5RQlakFUQdmGFtspRXCPayjRa3T6pNfo9Bqd3qIrQ2__PfBx5CGrAnzYACjfdPYQdbIeJgu9j2Cz7oN_Sv8vZxquVQ</recordid><startdate>20210521</startdate><enddate>20210521</enddate><creator>Byrne, Monika</creator><creator>Aughwane, Rosalind</creator><creator>James, Joanna L</creator><creator>Hutchinson, J Ciaran</creator><creator>Arthurs, Owen J</creator><creator>Sebire, Neil J</creator><creator>Ourselin, Sebastien</creator><creator>David, Anna L</creator><creator>Melbourne, Andrew</creator><creator>Clark, Alys R</creator><general>Elsevier Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20210521</creationdate><title>Structure-function relationships in the feto-placental circulation from in silico interpretation of micro-CT vascular structures</title><author>Byrne, Monika ; Aughwane, Rosalind ; James, Joanna L ; Hutchinson, J Ciaran ; Arthurs, Owen J ; Sebire, Neil J ; Ourselin, Sebastien ; David, Anna L ; Melbourne, Andrew ; Clark, Alys R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-8921fb74384ea396616309bd49133d14179d8f90c52e06d470a6a87acd238fab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Computational model</topic><topic>Haemodynamics</topic><topic>Micro-CT</topic><topic>Placenta</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Byrne, Monika</creatorcontrib><creatorcontrib>Aughwane, Rosalind</creatorcontrib><creatorcontrib>James, Joanna L</creatorcontrib><creatorcontrib>Hutchinson, J Ciaran</creatorcontrib><creatorcontrib>Arthurs, Owen J</creatorcontrib><creatorcontrib>Sebire, Neil J</creatorcontrib><creatorcontrib>Ourselin, Sebastien</creatorcontrib><creatorcontrib>David, Anna L</creatorcontrib><creatorcontrib>Melbourne, Andrew</creatorcontrib><creatorcontrib>Clark, Alys R</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of theoretical biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Byrne, Monika</au><au>Aughwane, Rosalind</au><au>James, Joanna L</au><au>Hutchinson, J Ciaran</au><au>Arthurs, Owen J</au><au>Sebire, Neil J</au><au>Ourselin, Sebastien</au><au>David, Anna L</au><au>Melbourne, Andrew</au><au>Clark, Alys R</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Structure-function relationships in the feto-placental circulation from in silico interpretation of micro-CT vascular structures</atitle><jtitle>Journal of theoretical biology</jtitle><addtitle>J Theor Biol</addtitle><date>2021-05-21</date><risdate>2021</risdate><volume>517</volume><spage>110630</spage><epage>110630</epage><pages>110630-110630</pages><artnum>110630</artnum><issn>0022-5193</issn><eissn>1095-8541</eissn><abstract>•The placenta provides a crucial nutrient exchange surface between mother and fetus.•Delivered placentae exhibit a wide range of vascular branching properties.•Our image-to-model framework aims to relate vascular branching to resistance.•Macro-scale vascular heterogeneities may indicate risk of elevated resistance.•Anastomoses between umbilical arteries mitigate impact of vascular heterogeneity.
A well-functioning placenta is critical for healthy fetal development, as the placenta brings fetal blood in close contact with nutrient rich maternal blood, enabling exchange of nutrients and waste between mother and fetus. The feto-placental circulation forms a complex branching structure, providing blood to fetal capillaries, which must receive sufficient blood flow to ensure effective exchange, but at a low enough pressure to prevent damage to placental circulatory structures. The branching structure of the feto-placental circulation is known to be altered in complications such as fetal growth restriction, and the presence of regions of vascular dysfunction (such as hypovascularity or thrombosis) are proposed to elevate risk of placental pathology. Here we present a methodology to combine micro-computed tomography and computational model-based analysis of the branching structure of the feto-placental circulation in ex vivo placentae from normal term pregnancies. We analyse how vascular structure relates to function in this key organ of pregnancy; demonstrating that there is a ‘resilience’ to placental vascular structure–function relationships. We find that placentae with variable chorionic vascular structures, both with and without a Hyrtl’s anastomosis between the umbilical arteries, and those with multiple regions of poorly vascularised tissue are able to function with a normal vascular resistance. Our models also predict that by progressively introducing local heterogeneity in placental vascular structure, large increases in feto-placental vascular resistances are induced. This suggests that localised heterogeneities in placental structure could potentially provide an indicator of increased risk of placental dysfunction.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>33607145</pmid><doi>10.1016/j.jtbi.2021.110630</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Computational model Haemodynamics Micro-CT Placenta |
title | Structure-function relationships in the feto-placental circulation from in silico interpretation of micro-CT vascular structures |
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