A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration.
The development of a functional cardiovascular system ensures a sustainable oxygen, nutrient and hormone delivery system for successful embryonic development and homeostasis in adulthood. While early vessels are formed by biochemical signaling and genetic programming, the onset of blood flow provide...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2023-12-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011665&type=printable |
| _version_ | 1827060917966209024 |
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| author | Swe Soe Maung Ye Li-Kun Phng |
| author_facet | Swe Soe Maung Ye Li-Kun Phng |
| author_sort | Swe Soe Maung Ye |
| collection | DOAJ |
| description | The development of a functional cardiovascular system ensures a sustainable oxygen, nutrient and hormone delivery system for successful embryonic development and homeostasis in adulthood. While early vessels are formed by biochemical signaling and genetic programming, the onset of blood flow provides mechanical cues that participate in vascular remodeling of the embryonic vascular system. The zebrafish is a prolific animal model for studying the quantitative relationship between blood flow and vascular morphogenesis due to a combination of favorable factors including blood flow visualization in optically transparent larvae. In this study, we have developed a cell-and-plasma blood transport model using computational fluid dynamics (CFD) to understand how red blood cell (RBC) partitioning affect lumen wall shear stress (WSS) and blood pressure in zebrafish trunk blood vascular networks with altered rheology and morphology. By performing live imaging of embryos with reduced hematocrit, we discovered that cardiac output and caudal artery flow rates were maintained. These adaptation trends were recapitulated in our CFD models, which showed reduction in network WSS via viscosity reduction in the caudal artery/vein and via pressure gradient weakening in the intersegmental vessels (ISVs). Embryos with experimentally reduced lumen diameter showed reduced cardiac output and caudal artery flow rate. Factoring in this trend into our CFD models, simulations highlighted that lumen diameter reduction increased vessel WSS but this increase was mitigated by flow reduction due to the adaptive network pressure gradient weakening. Additionally, hypothetical network CFD models with different vessel lumen diameter distribution characteristics indicated the significance of axial variation in lumen diameter and cross-sectional shape for establishing physiological WSS gradients along ISVs. In summary, our work demonstrates how both experiment-driven and hypothetical CFD modeling can be employed for the study of blood flow physiology during vascular remodeling. |
| first_indexed | 2024-03-08T19:58:06Z |
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| id | doaj.art-5d7563d24453493ca876cd1f490d542f |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2025-02-18T19:15:36Z |
| publishDate | 2023-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-5d7563d24453493ca876cd1f490d542f2024-10-20T05:31:26ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582023-12-011912e101166510.1371/journal.pcbi.1011665A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration.Swe Soe Maung YeLi-Kun PhngThe development of a functional cardiovascular system ensures a sustainable oxygen, nutrient and hormone delivery system for successful embryonic development and homeostasis in adulthood. While early vessels are formed by biochemical signaling and genetic programming, the onset of blood flow provides mechanical cues that participate in vascular remodeling of the embryonic vascular system. The zebrafish is a prolific animal model for studying the quantitative relationship between blood flow and vascular morphogenesis due to a combination of favorable factors including blood flow visualization in optically transparent larvae. In this study, we have developed a cell-and-plasma blood transport model using computational fluid dynamics (CFD) to understand how red blood cell (RBC) partitioning affect lumen wall shear stress (WSS) and blood pressure in zebrafish trunk blood vascular networks with altered rheology and morphology. By performing live imaging of embryos with reduced hematocrit, we discovered that cardiac output and caudal artery flow rates were maintained. These adaptation trends were recapitulated in our CFD models, which showed reduction in network WSS via viscosity reduction in the caudal artery/vein and via pressure gradient weakening in the intersegmental vessels (ISVs). Embryos with experimentally reduced lumen diameter showed reduced cardiac output and caudal artery flow rate. Factoring in this trend into our CFD models, simulations highlighted that lumen diameter reduction increased vessel WSS but this increase was mitigated by flow reduction due to the adaptive network pressure gradient weakening. Additionally, hypothetical network CFD models with different vessel lumen diameter distribution characteristics indicated the significance of axial variation in lumen diameter and cross-sectional shape for establishing physiological WSS gradients along ISVs. In summary, our work demonstrates how both experiment-driven and hypothetical CFD modeling can be employed for the study of blood flow physiology during vascular remodeling.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011665&type=printable |
| spellingShingle | Swe Soe Maung Ye Li-Kun Phng A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. PLoS Computational Biology |
| title | A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. |
| title_full | A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. |
| title_fullStr | A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. |
| title_full_unstemmed | A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. |
| title_short | A cell-and-plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration. |
| title_sort | cell and plasma numerical model reveals hemodynamic stress and flow adaptation in zebrafish microvessels after morphological alteration |
| url | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011665&type=printable |
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