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Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography

BACKGROUND: The kidney vasculature is exquisitely structured to orchestrate renal function. Structural profiling of the vasculature in intact rodent kidneys, has provided insights into renal haemodynamics and oxygenation, but has never been extended to the human kidney beyond a few vascular generati...

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Autores principales: Rahmani, Shahrokh, Jafree, Daniyal J., Lee, Peter D., Tafforeau, Paul, Jacob, Joseph, Bellier, Alexandre, Ackermann, Maximilian, Jonigk, Danny D., Shipley, Rebecca J., Long, David A., Walsh, Claire L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10081185/
https://www.ncbi.nlm.nih.gov/pubmed/37034801
http://dx.doi.org/10.1101/2023.03.28.534566
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author Rahmani, Shahrokh
Jafree, Daniyal J.
Lee, Peter D.
Tafforeau, Paul
Jacob, Joseph
Bellier, Alexandre
Ackermann, Maximilian
Jonigk, Danny D.
Shipley, Rebecca J.
Long, David A.
Walsh, Claire L.
author_facet Rahmani, Shahrokh
Jafree, Daniyal J.
Lee, Peter D.
Tafforeau, Paul
Jacob, Joseph
Bellier, Alexandre
Ackermann, Maximilian
Jonigk, Danny D.
Shipley, Rebecca J.
Long, David A.
Walsh, Claire L.
author_sort Rahmani, Shahrokh
collection PubMed
description BACKGROUND: The kidney vasculature is exquisitely structured to orchestrate renal function. Structural profiling of the vasculature in intact rodent kidneys, has provided insights into renal haemodynamics and oxygenation, but has never been extended to the human kidney beyond a few vascular generations. We hypothesised that synchrotron-based imaging of a human kidney would enable assessment of vasculature across the whole organ. METHODS: An intact kidney from a 63-year-old male was scanned using hierarchical phase-contrast tomography (HiP-CT), followed by semi-automated vessel segmentation and quantitative analysis. These data were compared to published micro-CT data of whole rat kidney. RESULTS: The intact human kidney vascular network was imaged with HiP-CT at 25 μm voxels, representing a 20-fold increase in resolution compared to clinical CT scanners. Our comparative quantitative analysis revealed the number of vessel generations, vascular asymmetry and a structural organisation optimised for minimal resistance to flow, are conserved between species, whereas the normalised radii are not. We further demonstrate regional heterogeneity in vessel geometry between renal cortex, medulla, and hilum, showing how the distance between vessels provides a structural basis for renal oxygenation and hypoxia. CONCLUSIONS: Through the application of HiP-CT, we have provided the first quantification of the human renal arterial network, with a resolution comparable to that of light microscopy yet at a scale several orders of magnitude larger than that of a renal punch biopsy. Our findings bridge anatomical scales, profiling blood vessels across the intact human kidney, with implications for renal physiology, biophysical modelling, and tissue engineering.
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spelling pubmed-100811852023-04-08 Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography Rahmani, Shahrokh Jafree, Daniyal J. Lee, Peter D. Tafforeau, Paul Jacob, Joseph Bellier, Alexandre Ackermann, Maximilian Jonigk, Danny D. Shipley, Rebecca J. Long, David A. Walsh, Claire L. bioRxiv Article BACKGROUND: The kidney vasculature is exquisitely structured to orchestrate renal function. Structural profiling of the vasculature in intact rodent kidneys, has provided insights into renal haemodynamics and oxygenation, but has never been extended to the human kidney beyond a few vascular generations. We hypothesised that synchrotron-based imaging of a human kidney would enable assessment of vasculature across the whole organ. METHODS: An intact kidney from a 63-year-old male was scanned using hierarchical phase-contrast tomography (HiP-CT), followed by semi-automated vessel segmentation and quantitative analysis. These data were compared to published micro-CT data of whole rat kidney. RESULTS: The intact human kidney vascular network was imaged with HiP-CT at 25 μm voxels, representing a 20-fold increase in resolution compared to clinical CT scanners. Our comparative quantitative analysis revealed the number of vessel generations, vascular asymmetry and a structural organisation optimised for minimal resistance to flow, are conserved between species, whereas the normalised radii are not. We further demonstrate regional heterogeneity in vessel geometry between renal cortex, medulla, and hilum, showing how the distance between vessels provides a structural basis for renal oxygenation and hypoxia. CONCLUSIONS: Through the application of HiP-CT, we have provided the first quantification of the human renal arterial network, with a resolution comparable to that of light microscopy yet at a scale several orders of magnitude larger than that of a renal punch biopsy. Our findings bridge anatomical scales, profiling blood vessels across the intact human kidney, with implications for renal physiology, biophysical modelling, and tissue engineering. Cold Spring Harbor Laboratory 2023-03-29 /pmc/articles/PMC10081185/ /pubmed/37034801 http://dx.doi.org/10.1101/2023.03.28.534566 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Rahmani, Shahrokh
Jafree, Daniyal J.
Lee, Peter D.
Tafforeau, Paul
Jacob, Joseph
Bellier, Alexandre
Ackermann, Maximilian
Jonigk, Danny D.
Shipley, Rebecca J.
Long, David A.
Walsh, Claire L.
Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title_full Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title_fullStr Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title_full_unstemmed Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title_short Micro to macro scale analysis of the intact human renal arterial tree with Synchrotron Tomography
title_sort micro to macro scale analysis of the intact human renal arterial tree with synchrotron tomography
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10081185/
https://www.ncbi.nlm.nih.gov/pubmed/37034801
http://dx.doi.org/10.1101/2023.03.28.534566
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