Abstract The endothelial lining of blood vessels
presents a large surface area for exchange of materials
between blood and tissues, and is critically involved in
many other processes such as regulation of blood flow,
inflammatory responses and blood coagulation. It has
long been known that the luminal surface of the endothe-
lium is lined with a glycocalyx, a layer of membrane-
bound macromolecules which has been determined by
electron microscopy to be several tens of nanometers
thick. However, investigations in vivo have indicated the
presence of a much thicker endothelial surface layer
(ESL), with an estimated thickness ranging from 0.5 μm
to over 1 μm, that restricts the flow of plasma and can
exclude red blood cells and some macromolecular sol-
utes. The evidence for the existence of the ESL, hypoth-
eses about its composition and biophysical properties, its
relevance to physiological processes, and its possible
clinical implications are considered in this review.
Key words Biophysical properties · Endothelial surface
layer · Fluid and solute exchange
Evidence for the existence
of the endothelial surface layer
Introduction
By extrapolating from data of Mall [63] on the anatomi-
cal dimensions of the vascular system in the canine in-
testine [48, 92], the total area of the blood/endothelium
interface in humans can be estimated to be about 350 m
2
.
For an estimated average endothelial thickness of about
0.3 μm, this corresponds to a total endothelial mass of
only 2245110 g. Nevertheless, the endothelium is by no
means just a passive membrane or barrier between blood
and tissues. On the contrary, it is actively involved in
many functions, such as the control and regulation of
vascular tone, fluid and solute exchange, haemostasis
and coagulation and inflammatory responses. Most of
these functions depend critically on phenomena occur-
ring at the endothelial surface in the vascular lumen. The
physical and chemical nature of the surface presented by
endothelial cells to the flowing blood can therefore be
assumed to influence many of these aspects of vascular
function.
The concept that vessel walls are lined with an extra-
cellular layer of membrane-bound substances dates back
more than 50 years. Initially, studies of endothelial per-
meability initiated an interest in the structure and com-
position of the material on the endothelial surface and in
the inter-endothelial clefts. Danielli [28] and Chambers
and Zweifach [18] introduced the concept of a thin non-
cellular layer on the endothelial surface (endocapillary
layer) which was thought to include adsorbed plasma
proteins. Direct observation of this layer proved to be
technically impossible. However, during perfusion of the
frog mesentery with a Ringer’s solution containing
Evans blue, which has a high affinity for albumin,
Chambers and Zweifach [18] observed “thin strands and
sheets of a faintly colored blue, translucent material …
sloughing off the inner surface of the capillary.” About
20 years later, Copley [21, 22] studied the endotheli-
um–plasma interface and developed a concept (Fig. 1) in
which the endothelial surface is covered by a thin molec-
ular layer and an immobile sheet of plasma. The exis-
tence of the latter was inferred from intravital micro-
scopic experiments in the hamster cheek pouch [23]. Af-
ter intravenous injection of a dye (pontamine sky blue)
an unstained plasmatic zone adjacent to the endothelial
surface was observed.
In 1966, Luft [62] used ruthenium red staining for an
electron microscopic study of the endothelial surface.
A.R. Pries · P. Gaehtgens
Dept. of Physiology, Freie Universität Berlin,
Arnimallee 22, 14195 Berlin, Germany
A.R. Pries
Deutsches Herzzentrum Berlin,
Augustenburger Platz 1, 13353 Berlin, Germany
T.W. Secomb
Dept. of Physiology, University of Arizona,
Tucson, AZ 85724, USA
Pflügers Arch – Eur J Physiol (2000) 440:653–666
DOI 10.1007/s004240000307
INVITED REVIEW
A.R. Pries · T.W. Secomb · P. Gaehtgens
The endothelial surface layer
Received: 8 December 1999 / Received after revision: 3 March 2000Accepted: 6 March 2000 / Published online: 21 April 2000
© Springer-Verlag 2000