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Feto-placental vascular structure and in silico haemodynamics: Of mice, rats, and human
The complex arborization of the feto-placental vasculature is crucial for optimal fetal nutrition, waste exchange and ultimately, development. Ethical and experimental limitations constrain research into the human placenta, hence experimental animal models such as mice and rats, are crucial to under...
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Published in: | Placenta (Eastbourne) 2024-12, Vol.158, p.175-184 |
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creator | Bappoo, Nikhilesh Tongpob, Yutthapong Hakim, Matina Myers, Jenny Panting, Emma Chapman, Karen E. Thomson, Adrian J.W. Moran, Carmel M. Kelsey, Lachlan J. Srinivasan, Vijayalakshmi James, Joanna L. Clark, Alys R. Doyle, Barry J. Wyrwoll, Caitlin S. |
description | The complex arborization of the feto-placental vasculature is crucial for optimal fetal nutrition, waste exchange and ultimately, development. Ethical and experimental limitations constrain research into the human placenta, hence experimental animal models such as mice and rats, are crucial to understand placental function. It is unclear how well the mouse and rat feto-placental vascular structure emulates human. Moreover, the implications of differences in vascular structure, especially in arborization, for placental function remain unclear.
We use micro-computed tomography imaging, high frequency Doppler ultrasound and computational fluid dynamics to characterize feto-placental vasculature structure and haemodynamics in mice, rats, and human.
Our data suggest that despite structural differences between rat and mouse placenta, haemodynamics are similar and that both hold applicability to investigating feto-placental structure and function. We show that human cotyledons demonstrate vascularity-dependent haemodynamic behaviour (including flow deceleration and oxygen exchange) similar to rodents and can be analysed in the same spectrum as rodents. Finally, we show strong structure-function relationships when interspecies datasets are combined; notably, we demonstrate that surrogate measures such as vascularity, can be used to estimate placental oxygen exchange function.
Pre-clinical placental research utilising rat and mouse placentae to understand the impact of feto-placental arborization on placental function and fetal development can inform the human context.
•We compared feto-placental vascular structure of mouse, rat, and human.•Feto-placental vascular interspecies variation does not impact oxygen delivery.•For feto-placental vasculature, the mouse and rat are useful preclinical models. |
doi_str_mv | 10.1016/j.placenta.2024.10.020 |
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We use micro-computed tomography imaging, high frequency Doppler ultrasound and computational fluid dynamics to characterize feto-placental vasculature structure and haemodynamics in mice, rats, and human.
Our data suggest that despite structural differences between rat and mouse placenta, haemodynamics are similar and that both hold applicability to investigating feto-placental structure and function. We show that human cotyledons demonstrate vascularity-dependent haemodynamic behaviour (including flow deceleration and oxygen exchange) similar to rodents and can be analysed in the same spectrum as rodents. Finally, we show strong structure-function relationships when interspecies datasets are combined; notably, we demonstrate that surrogate measures such as vascularity, can be used to estimate placental oxygen exchange function.
Pre-clinical placental research utilising rat and mouse placentae to understand the impact of feto-placental arborization on placental function and fetal development can inform the human context.
•We compared feto-placental vascular structure of mouse, rat, and human.•Feto-placental vascular interspecies variation does not impact oxygen delivery.•For feto-placental vasculature, the mouse and rat are useful preclinical models.</description><identifier>ISSN: 0143-4004</identifier><identifier>ISSN: 1532-3102</identifier><identifier>EISSN: 1532-3102</identifier><identifier>DOI: 10.1016/j.placenta.2024.10.020</identifier><identifier>PMID: 39476476</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>Animals ; Computer Simulation ; Female ; Hemodynamics - physiology ; Human ; Humans ; Imaging ; Mice ; Mouse ; Placenta ; Placenta - blood supply ; Placenta - physiology ; Placental Circulation - physiology ; Pregnancy ; Rat ; Rats ; Vasculature ; X-Ray Microtomography</subject><ispartof>Placenta (Eastbourne), 2024-12, Vol.158, p.175-184</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c293t-c9d28f3c68d946b56a163ad3b01ceb54b59aed39852b95252b7858645b9e25d33</cites><orcidid>0000-0002-5746-5680</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39476476$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bappoo, Nikhilesh</creatorcontrib><creatorcontrib>Tongpob, Yutthapong</creatorcontrib><creatorcontrib>Hakim, Matina</creatorcontrib><creatorcontrib>Myers, Jenny</creatorcontrib><creatorcontrib>Panting, Emma</creatorcontrib><creatorcontrib>Chapman, Karen E.</creatorcontrib><creatorcontrib>Thomson, Adrian J.W.</creatorcontrib><creatorcontrib>Moran, Carmel M.</creatorcontrib><creatorcontrib>Kelsey, Lachlan J.</creatorcontrib><creatorcontrib>Srinivasan, Vijayalakshmi</creatorcontrib><creatorcontrib>James, Joanna L.</creatorcontrib><creatorcontrib>Clark, Alys R.</creatorcontrib><creatorcontrib>Doyle, Barry J.</creatorcontrib><creatorcontrib>Wyrwoll, Caitlin S.</creatorcontrib><title>Feto-placental vascular structure and in silico haemodynamics: Of mice, rats, and human</title><title>Placenta (Eastbourne)</title><addtitle>Placenta</addtitle><description>The complex arborization of the feto-placental vasculature is crucial for optimal fetal nutrition, waste exchange and ultimately, development. Ethical and experimental limitations constrain research into the human placenta, hence experimental animal models such as mice and rats, are crucial to understand placental function. It is unclear how well the mouse and rat feto-placental vascular structure emulates human. Moreover, the implications of differences in vascular structure, especially in arborization, for placental function remain unclear.
We use micro-computed tomography imaging, high frequency Doppler ultrasound and computational fluid dynamics to characterize feto-placental vasculature structure and haemodynamics in mice, rats, and human.
Our data suggest that despite structural differences between rat and mouse placenta, haemodynamics are similar and that both hold applicability to investigating feto-placental structure and function. We show that human cotyledons demonstrate vascularity-dependent haemodynamic behaviour (including flow deceleration and oxygen exchange) similar to rodents and can be analysed in the same spectrum as rodents. Finally, we show strong structure-function relationships when interspecies datasets are combined; notably, we demonstrate that surrogate measures such as vascularity, can be used to estimate placental oxygen exchange function.
Pre-clinical placental research utilising rat and mouse placentae to understand the impact of feto-placental arborization on placental function and fetal development can inform the human context.
•We compared feto-placental vascular structure of mouse, rat, and human.•Feto-placental vascular interspecies variation does not impact oxygen delivery.•For feto-placental vasculature, the mouse and rat are useful preclinical models.</description><subject>Animals</subject><subject>Computer Simulation</subject><subject>Female</subject><subject>Hemodynamics - physiology</subject><subject>Human</subject><subject>Humans</subject><subject>Imaging</subject><subject>Mice</subject><subject>Mouse</subject><subject>Placenta</subject><subject>Placenta - blood supply</subject><subject>Placenta - physiology</subject><subject>Placental Circulation - physiology</subject><subject>Pregnancy</subject><subject>Rat</subject><subject>Rats</subject><subject>Vasculature</subject><subject>X-Ray Microtomography</subject><issn>0143-4004</issn><issn>1532-3102</issn><issn>1532-3102</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkEtLAzEQgIMoWh9_QXL00K15d-NJKb6g0IviMWSTKabsoya7hf57U2u9CmEyDN_MMB9C15RMKKHqdjVZ19ZB29sJI0zk4oQwcoRGVHJWcErYMRoRKnghCBFn6DylFSFEC8pO0RnXYqryG6GPJ-i74jCrxhub3FDbiFMfB9cPEbBtPQ4tTqEOrsOfFprOb1vbBJfu8GKJcwJjHG2fxj_s59DY9hKdLG2d4Or3v0DvT49vs5divnh-nT3MC8c07wunPSuX3KnSa6EqqSxV3HpeEeqgkqKS2oLnupSs0pLlOC1lqYSsNDDpOb9AN_u569h9DZB604TkoK5tC92QDKeMKT4lgmRU7VEXu5QiLM06hsbGraHE7KSalTmIMDupu3qWmhuvf3cMVQP-r-1gMQP3ewDypZsA0SQXoHXgQwTXG9-F_3Z8AzDciyI</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Bappoo, Nikhilesh</creator><creator>Tongpob, Yutthapong</creator><creator>Hakim, Matina</creator><creator>Myers, Jenny</creator><creator>Panting, Emma</creator><creator>Chapman, Karen E.</creator><creator>Thomson, Adrian J.W.</creator><creator>Moran, Carmel M.</creator><creator>Kelsey, Lachlan J.</creator><creator>Srinivasan, Vijayalakshmi</creator><creator>James, Joanna L.</creator><creator>Clark, Alys R.</creator><creator>Doyle, Barry J.</creator><creator>Wyrwoll, Caitlin S.</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5746-5680</orcidid></search><sort><creationdate>202412</creationdate><title>Feto-placental vascular structure and in silico haemodynamics: Of mice, rats, and human</title><author>Bappoo, Nikhilesh ; Tongpob, Yutthapong ; Hakim, Matina ; Myers, Jenny ; Panting, Emma ; Chapman, Karen E. ; Thomson, Adrian J.W. ; Moran, Carmel M. ; Kelsey, Lachlan J. ; Srinivasan, Vijayalakshmi ; James, Joanna L. ; Clark, Alys R. ; Doyle, Barry J. ; Wyrwoll, Caitlin S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c293t-c9d28f3c68d946b56a163ad3b01ceb54b59aed39852b95252b7858645b9e25d33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Computer Simulation</topic><topic>Female</topic><topic>Hemodynamics - physiology</topic><topic>Human</topic><topic>Humans</topic><topic>Imaging</topic><topic>Mice</topic><topic>Mouse</topic><topic>Placenta</topic><topic>Placenta - blood supply</topic><topic>Placenta - physiology</topic><topic>Placental Circulation - physiology</topic><topic>Pregnancy</topic><topic>Rat</topic><topic>Rats</topic><topic>Vasculature</topic><topic>X-Ray Microtomography</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bappoo, Nikhilesh</creatorcontrib><creatorcontrib>Tongpob, Yutthapong</creatorcontrib><creatorcontrib>Hakim, Matina</creatorcontrib><creatorcontrib>Myers, Jenny</creatorcontrib><creatorcontrib>Panting, Emma</creatorcontrib><creatorcontrib>Chapman, Karen E.</creatorcontrib><creatorcontrib>Thomson, Adrian J.W.</creatorcontrib><creatorcontrib>Moran, Carmel M.</creatorcontrib><creatorcontrib>Kelsey, Lachlan J.</creatorcontrib><creatorcontrib>Srinivasan, Vijayalakshmi</creatorcontrib><creatorcontrib>James, Joanna L.</creatorcontrib><creatorcontrib>Clark, Alys R.</creatorcontrib><creatorcontrib>Doyle, Barry J.</creatorcontrib><creatorcontrib>Wyrwoll, Caitlin S.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Placenta (Eastbourne)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bappoo, Nikhilesh</au><au>Tongpob, Yutthapong</au><au>Hakim, Matina</au><au>Myers, Jenny</au><au>Panting, Emma</au><au>Chapman, Karen E.</au><au>Thomson, Adrian J.W.</au><au>Moran, Carmel M.</au><au>Kelsey, Lachlan J.</au><au>Srinivasan, Vijayalakshmi</au><au>James, Joanna L.</au><au>Clark, Alys R.</au><au>Doyle, Barry J.</au><au>Wyrwoll, Caitlin S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Feto-placental vascular structure and in silico haemodynamics: Of mice, rats, and human</atitle><jtitle>Placenta (Eastbourne)</jtitle><addtitle>Placenta</addtitle><date>2024-12</date><risdate>2024</risdate><volume>158</volume><spage>175</spage><epage>184</epage><pages>175-184</pages><issn>0143-4004</issn><issn>1532-3102</issn><eissn>1532-3102</eissn><abstract>The complex arborization of the feto-placental vasculature is crucial for optimal fetal nutrition, waste exchange and ultimately, development. Ethical and experimental limitations constrain research into the human placenta, hence experimental animal models such as mice and rats, are crucial to understand placental function. It is unclear how well the mouse and rat feto-placental vascular structure emulates human. Moreover, the implications of differences in vascular structure, especially in arborization, for placental function remain unclear.
We use micro-computed tomography imaging, high frequency Doppler ultrasound and computational fluid dynamics to characterize feto-placental vasculature structure and haemodynamics in mice, rats, and human.
Our data suggest that despite structural differences between rat and mouse placenta, haemodynamics are similar and that both hold applicability to investigating feto-placental structure and function. We show that human cotyledons demonstrate vascularity-dependent haemodynamic behaviour (including flow deceleration and oxygen exchange) similar to rodents and can be analysed in the same spectrum as rodents. Finally, we show strong structure-function relationships when interspecies datasets are combined; notably, we demonstrate that surrogate measures such as vascularity, can be used to estimate placental oxygen exchange function.
Pre-clinical placental research utilising rat and mouse placentae to understand the impact of feto-placental arborization on placental function and fetal development can inform the human context.
•We compared feto-placental vascular structure of mouse, rat, and human.•Feto-placental vascular interspecies variation does not impact oxygen delivery.•For feto-placental vasculature, the mouse and rat are useful preclinical models.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>39476476</pmid><doi>10.1016/j.placenta.2024.10.020</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-5746-5680</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Computer Simulation Female Hemodynamics - physiology Human Humans Imaging Mice Mouse Placenta Placenta - blood supply Placenta - physiology Placental Circulation - physiology Pregnancy Rat Rats Vasculature X-Ray Microtomography |
title | Feto-placental vascular structure and in silico haemodynamics: Of mice, rats, and human |
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