Elsevier

Placenta

Volume 14, Issue 5, September–October 1993, Pages 591-604
Placenta

Branching patterns of human placental villous trees: Perspectives of topological analysis

https://doi.org/10.1016/S0143-4004(05)80212-7Get rights and content

Summary

Topological analysis was applied to investigate the branching pattern of three specimens obtained from early human placenta (6, 9, and 16 weeks p.m.) reconstructed on the basis of semi-thin sections. Centripetal Horton-Strahler and centrifugal branching order nomenclature was used for topological description of the analysed tree-like structures. Bifurcation ratio and vertex ratio were determined for all three cases and were found to be relatively constant. It was shown that branching pattern is closely related to the model of random segment branching that implicates a high level of asymmetry and a small level of space limitation for branching. The significance of this approach for the analysis of development of the villous tree, for the analysis of mesenchymal villous heterogeneity and for the estimation of physiological parameters for fetoplacental exchange is discussed. We suggest that topological analysis can lead to a new quantitative classification of branching patterns of the human placental villous trees in normal and pathologic pregnancies.

References (56)

  • BoydJ.D. et al.
  • BurtonG.J.

    Intervillous connections in the mature human placenta: instances of synctial fusion or section of artefacts?

    Journal of Anatomy

    (1986)
  • BurtonG.J.

    Scanning electron microscopy of intervillous connections in the mature human placenta

    Journal of Anatomy

    (1986)
  • BurtonG.J.

    The fine structure of the human placental villus as revealed by scanning electron microscopy

    Scanning Microscopy

    (1987)
  • BurtonG.J. et al.

    A technique for correlative scanning and transmission electron microscopy of individual human placental villi: an example demonstrating syncytial sprouts inearly gestation

    Scanning Microscopy

    (1991)
  • CastellucciM. et al.

    The development of the placental villous tree

    Anatomy and Embryology

    (1990)
  • CastellucciM. et al.

    The human placenta: a model for tenascin expression

    Histochemistry

    (1991)
  • DemirR. et al.

    Fetal vasculogenesis and angiogenesis in human placental villi

    Acta Anatomica

    (1989)
  • FoxH.
  • Garcia-RuizJ.M. et al.

    Fractal trees and Horton's Laws

    Mathematical Geology

    (1992)
  • GuiotC. et al.

    Modelling the feto-placental circulation, I: a distributed network predicting umbilical haemodynamics throughout pregnancy

    Ultrasound in Medicine and Biology

    (1992)
  • HollingworthT. et al.

    Network analysis of dendritic fields of pyramidal cells in the cerebellum of the rat

    Philosophical Transactions of the Royal Society of London. B: Biological Science

    (1975)
  • HortonR.E.

    Erosioal development of streams and their drainage basins

    Bulletin of the Geological Society of America

    (1945)
  • HolmgrenK. et al.

    Angiogenesis during human extraembryonic development involves the spatiotemporal control of PDGF ligand receptor gene expression

    Development

    (1991)
  • IkléF.A.

    Trophoblastzellen im strömenden Blut

    Schweizerische Medizinische Wochenschrift

    (1961)
  • KaufmannP.

    Development and differentiation of the human placental villous tree

    Bibliotheca Anatomica

    (1982)
  • KaufmannP. et al.

    Development and differentiation of the human placental villous tree

    Journal of the Tokyo Medical College

    (1990)
  • KaufmannP. et al.

    Features of growth of human placental villous trees

    Placenta

    (1991)
  • Cited by (28)

    • The placenta in fetal growth restriction: What is going wrong?

      2020, Placenta
      Citation Excerpt :

      Death of these contractile stromal cells could contribute to decreased vascular compliance and increased vascular resistance seen in FGR placentae [64,65]. Early in gestation, cytotrophoblast proliferation facilitates villus growth via random segmental branching (new villi may emerge at any segment of the existing tree with equal probability), resulting in extensive linear growth of terminal villi from the second trimester onwards [66]. Later in gestation, terminal villus generation predominantly occurs due to the expansion of fetal vessels, concurrent with a decrease in cytotrophoblast proliferation and increased apoptotic death towards term [67,68].

    • A multiscale model of placental oxygen exchange: The effect of villous tree structure on exchange efficiency

      2016, Journal of Theoretical Biology
      Citation Excerpt :

      Assuming that oxygenated maternal blood enters into the IVS at a normal rate, the decrease in oxygen uptake rate would give rise to a higher average pO2 in the IVS than in normal pregnancies, which is consistent with hyperoxia in the IVS as suggested by Kingdom et al. in IUGR placentas (Kingdom and Kaufmann, 1997). Model limitations: There are several studies which aim to quantify the branching properties of villous structures (Haeussner et al., 2014; Kosanke et al., 1993), and these studies are becoming increasingly quantitative allowing incorporation of branching and 3D rotation angles (Haeussner et al., 2014). Our branching villous model aims to match as closely as possible to these existing studies, in terms of measured tree properties including branch numbers and lengths.

    • Modeling the Variability of Shapes of a Human Placenta

      2008, Placenta
      Citation Excerpt :

      Irregularities in disk outline, umbilical cord insertion and in disk thickness are markers of fetal–placental environmental pathology, denoting variable placental arborization, and as such, deformation of normal placental growth resulting in an abnormal placental structure. The microscopic growth of the human placenta involves repeated branching, analogous to the roots of a tree; its mature arborization pattern is complex (e.g., [1–8]), so complex that it cannot be measured reliably even by expert, dedicated pediatric pathologists [9,10]. Just as the pattern of roots reflects the underlying soil's fertility and predicts the health of plants that depend on those roots for sustenance, placental arborization reflects the health of the maternal environment and impacts on fetal health [11].

    • The correlation between sampling site and gene expression in the term human placenta

      2005, Placenta
      Citation Excerpt :

      Lastly, we chose our sites based on an unbiased systematic sampling of different placental regions. Previous studies utilized other approaches to spatial analysis of placental histomorphology or function (for example, see Refs. [21–24]), and it is likely that different methodologies might influence the extent of gene expression changes. Transcript expression at the medio-basal region might be influenced by the location at the center of the placenta or by the proximity to the umbilical cord insertion.

    View all citing articles on Scopus
    *

    Preliminary data were presented at the 87th meeting of the anatomical Society (Mainz, FRG) (Mironov et al, 1992a) and at the 12th Rochester Trophoblast Conference (Rochester, NY, USA) (Mironov et al, 1992b).

    View full text