Structure and hemodynamics of vascular networks in the chorioallantoic membrane of the chicken

Martin Maibier, Bettina Reglin, Bianca Nitzsche, Weiwei Xiang, Wen Wei Rong, Björn Hoffmann, Valentin Djonov, Timothy W Secomb, Axel R. Pries

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

The chick chorioallantoic membrane (CAM) is extensively used as an in vivo model. Here, structure and hemodynamics of CAM vessel trees were analyzed and compared with predictions of Murray’s law. CAM microvascular networks of Hamburger-Hamilton stage 40 chick embryos were scanned by videomicroscopy. Three networks with ~3,800, 580, and 480 segments were digitally reconstructed, neglecting the capillary mesh. Vessel diameters (D) and segment lengths were measured, and generation numbers and junctional exponents at bifurcations were derived. In selected vessels, flow velocities (v) and hematocrit were measured. Hemodynamic simulations, incorporating the branching of capillaries from preterminal vessels, were used to estimate v, volume flow, shear stress (τ), and pressure for all segments of the largest network. For individual arteriovenous flow pathways, terminal arterial and venous generation numbers are negatively correlated, leading to low variability of total topological and morphological pathway lengths. Arteriolar velocity is proportional to diameter (vD1.03 measured, vD0.93 modeling), giving nearly uniform τ levels (τD0.05). Venular trees exhibit slightly higher exponents (vD1.3, τD0.38). Junctional exponents at divergent and convergent bifurcations were 2.05 ± 1.13 and 1.97 ± 0.95 (mean ± SD) in contrast to the value 3 predicted by Murray’s law. In accordance with Murray’s law, τ levels are (nearly) maintained in CAM arterial (venular) trees, suggesting vascular adaptation to shear stress. Arterial and venous trees show an interdigitating arrangement providing homogeneous flow pathway properties and have preterminal capillary branches. These properties may facilitate efficient oxygen exchange in the CAM during rapid embryonic growth.

Original languageEnglish (US)
Pages (from-to)H913-H926
JournalAmerican Journal of Physiology - Heart and Circulatory Physiology
Volume311
Issue number4
DOIs
StatePublished - 2016

Fingerprint

Chorioallantoic Membrane
Blood Vessels
Chickens
Hemodynamics
Video Microscopy
Chick Embryo
Microvessels
Hematocrit
Oxygen
Pressure
Growth

Keywords

  • Angiogenesis
  • Cardiovascular modeling
  • Chick embryo
  • Microcirculation
  • Murray’s law

ASJC Scopus subject areas

  • Physiology
  • Cardiology and Cardiovascular Medicine
  • Physiology (medical)

Cite this

Structure and hemodynamics of vascular networks in the chorioallantoic membrane of the chicken. / Maibier, Martin; Reglin, Bettina; Nitzsche, Bianca; Xiang, Weiwei; Rong, Wen Wei; Hoffmann, Björn; Djonov, Valentin; Secomb, Timothy W; Pries, Axel R.

In: American Journal of Physiology - Heart and Circulatory Physiology, Vol. 311, No. 4, 2016, p. H913-H926.

Research output: Contribution to journalArticle

Maibier, Martin ; Reglin, Bettina ; Nitzsche, Bianca ; Xiang, Weiwei ; Rong, Wen Wei ; Hoffmann, Björn ; Djonov, Valentin ; Secomb, Timothy W ; Pries, Axel R. / Structure and hemodynamics of vascular networks in the chorioallantoic membrane of the chicken. In: American Journal of Physiology - Heart and Circulatory Physiology. 2016 ; Vol. 311, No. 4. pp. H913-H926.
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AU - Reglin, Bettina

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AU - Hoffmann, Björn

AU - Djonov, Valentin

AU - Secomb, Timothy W

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AB - The chick chorioallantoic membrane (CAM) is extensively used as an in vivo model. Here, structure and hemodynamics of CAM vessel trees were analyzed and compared with predictions of Murray’s law. CAM microvascular networks of Hamburger-Hamilton stage 40 chick embryos were scanned by videomicroscopy. Three networks with ~3,800, 580, and 480 segments were digitally reconstructed, neglecting the capillary mesh. Vessel diameters (D) and segment lengths were measured, and generation numbers and junctional exponents at bifurcations were derived. In selected vessels, flow velocities (v) and hematocrit were measured. Hemodynamic simulations, incorporating the branching of capillaries from preterminal vessels, were used to estimate v, volume flow, shear stress (τ), and pressure for all segments of the largest network. For individual arteriovenous flow pathways, terminal arterial and venous generation numbers are negatively correlated, leading to low variability of total topological and morphological pathway lengths. Arteriolar velocity is proportional to diameter (vD1.03 measured, vD0.93 modeling), giving nearly uniform τ levels (τD0.05). Venular trees exhibit slightly higher exponents (vD1.3, τD0.38). Junctional exponents at divergent and convergent bifurcations were 2.05 ± 1.13 and 1.97 ± 0.95 (mean ± SD) in contrast to the value 3 predicted by Murray’s law. In accordance with Murray’s law, τ levels are (nearly) maintained in CAM arterial (venular) trees, suggesting vascular adaptation to shear stress. Arterial and venous trees show an interdigitating arrangement providing homogeneous flow pathway properties and have preterminal capillary branches. These properties may facilitate efficient oxygen exchange in the CAM during rapid embryonic growth.

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