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The fine structure of the arteriovenous anastomosis and its nerve supply in the human nasal respiratory mucosa.

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The Fine Structure of the Arteriovenous Anastomosis
and Its Nerve Supply in the Human
Nasal Respiratory Mucosa '
Department of Anatomy and Cell Biology, T h e School of Medicine,
University of Pittsburgh, Pittsburgh, Pennsylvania I521 3
The fine structure of the arteriovenous anastomosis was investigated
i n the normal human nasal mucosa. The tissues were fixed i n 2% osmic acid solution,
embedded in Epon and stained with uranyl acetate and lead citrate solutions.
It was found that the endothelial basement membrane of the arterial segment of
the anastomosis was discontinuous. The anastomosing artery possessed subendothelial
cushions of longitudinal smooth musculature which expanded into a thick uniform
layer before the artery joined the vein. The fine morphology of these muscle cells did
not show epitheloid modification. An elastic membrane of a peculiar structure separated the subendothelial musculature from that of the tunica media. The membrane
was continuous with the internal elastic membrane of the proximal artery and with the
adventitial elastic mesh of the vein. The anastomosis was supplied by a non-myelinated
periarterial nerve plexus which contained cholinergic and adrenergic axons characterized by agranular and fine granular vesicles respectively. The wall of the vein was
devoid of musculature and nerves. It mainly consisted of elastic meshes interspersed
with bundles of collagen fibers and occasional fibrocytes.
It was suggested that the musculature of the tunica media of the artery was controlled by the cholinergic and adrenergic nerves of the autonomic system, and by the
sensory nerves in the form of axons reflexes. The subendothelial musculature was
controlled by agents carried in blood and was not influenced by the adventitial nerves.
The blood vessels of the nose regulate the and is an extension of earlier investigations
size of the nasal passages and are involved in this series (Cauna, '70; Cauna et al.,
in the humidification and thermal adjust- '69; Cauna and Hinderer, '69).
ment of the inhaled air. The vascular bed
expands and contracts rhythmically probably due to the activities of the arterioThe material used in this study was obvenous anastomoses (Clark and Clark, tained during corrective surgery of the nose
'34). The vessels react vividly to various under block anesthesia with 2% Xplokinds of environmental stimuli, drugs and caine @ solution. 'Tissues came from seven
emotional conditions. They appear to be male and three female patients ranging in
under sympathetic and parasympathetic age from 16 to 48 years. They were fixed
control (Malcomson, '59). The existence in 1% osmic acid solution in phosphate
of the arteriovenous anastomoses in the buffer, embedded in Epon 812 and stained
human nose was denied as recently as 30 with uranyl acetate and lead citrate soluyears ago (Korner, '37). Subsequent work- tions (Cauna et al., '69). All illustrations in
ers, however, demonstrated these struc- this paper were taken from the septal mutures beyond dispute (Mark, '41; Fabbi cosa dorsal to the ~UCO-cutaneous
and Rossatti, '51; TemesrkkBsi, '69). Ros- of a male patient 46 years old.
satti ('54) further suggested that the orOBSERVATIONS
ganization and function of the anastomoses were different in the erectile tissue over
The arteriovenous anastomoses were frethe conchae and in the septal mucosa quently encountered in the deeper layer of
which did not possess true cavernous si- the nasal lining, usually near the nasal
nuses. The present work is part of a correReceived Feb. 9. '70. Accewted Awr. 8 , '70.
lative study of the fine morphology, histo1 This study was supported by Public Health Service
chemistry and functions of the nasal lining grant NB 04147.
ANAT.REC., 168: 9-22.
glands. The anastomosing vessels were tortuous to a varying degree. Sometimes they
resembled simple glomeruli, but they were
devoid of distinct fibrous capsules. The anastomosing arteries were characterized by
the appearance in their walls of fascicles
of longitudinal smooth muscle cells located
between the endothelial lining and the internal elastic membrane ( M in fig. 1).
Nearer the anastomosis, the subendothelial
Fig. 1 Transverse section of a n artery near its tmastomosis with the vein. Its tunica
intima has acquired an incomplete layer of longitudinal smooth muscle fibers ( M ) located
between the internal elastic membrane (El) and the endothelium (cf. with M in fig. 2 ) .
Tm, tunica media; G, acinus of a nasal gland. Osmium fixed tissue embedded in Epon, 1 p
thick section stained with toluidine blue solution. x 400.
Fig. 2 Transverse section of the arteriovenous anastomosis. M, longitudinal subendothelial smooth muscle cell layer (cf. with M in fig. 1). El, elastic membrane, continuous with
the internal elastic membrane of the proximal segment of the artery (cf. with El in fig. 1);
Tm, tunica media ending at h, a short distance before the junction with the vein (V). Osmium fixed tissue embedded in Epon, 1 p thick section stained with toluidine blue solution.
X 400.
musculature became thick and uniformly
distributed around the lumen of the artery
(M in fig. 2). The transition of the thick
walled artery into the thin walled vein was
abrupt ( V in figs. 2, 8). Both segments
showed unusual fine morphology. The arterial segment appeared to possess a dual
nerve supply.
The arterial segment
The arterial segment possessed a closed
endothelial lining which was supported externally by a discontinuous basement membrane. The latter filled the wide interval
between the endothelial tube and the longitudinal muscle cell layer and had the
appearance of a loose network which was
traversed by large and irregular passages
(BM i n fig. 3 ) .
The subendothelial muscle cells were
loosely arranged ( m in figs. 4, 5). The intervals usually contained collagen fibers
of longitudinal orientation ( A i n fig. 4 ) .
The cells that were nearest to the tunica
media were also spaced by extensions of
the elastic membrane and by occasional
fibrocytes (Lam and F in fig. 5). All muscle
cells appeared to be interconnected across
the spaces by appositional junctions (Jc in
fig. 4). Their basement membrane was
thick and formed a continuous system extending from cell to cell over the junctional
areas (bm i n fig. 4 ) . Only the luminal aspects of the innermost muscle cells were
devoid of it, and were related to the modified basement membrane of the endothelial
tube (cf. bm and BM in fig. 3 ) .
Fig. 3 Tunica intima of the arterial segment of the anastomosis. L, lumen; End, endothelial cell;
EM, zone of the modified endothelial basement membrane; m, subendothelial muscle cell; bm, basement membrane of the subendothelial musculature. ?: 25,000.
Fig. 4 Subendothelial smooth muscle cells ( m ) spaced by intervals (A) and interconnected by appositional junctions (Jc) ; bm, basement membrane system of the musculature. X 20,000.
The elastic membrane that separated the
subendothelial musculature from the tunica media was found to be a continuation
of the internal elastic membrane of the
artery that gave rise to the anastomosis (cf.
El in figs. 1, 2). Distally the membrane
became continuous with the adventitial
elastic mesh of the vein (el. in figs. 8 , 10).
The arterial elastic membrane had a characteristic fine structure (El in fig. 5). Its
outer zone consisted of a continuous elastic lamella, while the inner zone contained
fine branching elastic fibers. The latter
were finest on the innermost aspect of the
membrane (cf. El and el in fig. 6). The
inner zone also contained collagen fibers,
microfibrils and some peculiar fluted fibers
that were not observed elsewhere (unlabelled arrows in fig. 6 ) . Scattered
throughout the elastic membrane and its
continuation into the wall of the vein were
electron dense spherical granules ranging
from approximately 200 A to 0.5 in diameter ( G in figs. 5 , 6 , 7, 10). They showed an
irregular grainy substructure under high
magnification both in stained and unstained sections. The external surface of
the elastic membrane facing the tunica
media was smooth; that facing the subendothelial musculature appeared uneven
and was frequently laminated. Some laminae extended into the subendothelial musculature for a considerable distance (Lam
in fig. 5). On approaching the junction between the artery and the vein, the elastic
membrane underwent a gradual change.
The outer elastic lamina became progressively thinner and fragmented (El in fig.
7), and it disappeared altogether without
reaching the vein. The inner zone of the
Fig. 5 Elastic membrane ( E l ) of the arterial segment of the arteriovenous anastomosis located between the tunica media (Media) and the subendothelial smooth muscle cells ( m ) . G , granules in the
elastic membrane; Lam, elastic lamina extending into the subendothelial muscle cell layers; F, part of a
fibrocyte. ?< 12,000.
Fig. 6 Segment of the elastic membrane (cf. with El in fig. 5 ) . The outer zone consists of a continuous elastic lamina (El), the inner zone contains fine elastic fibers (el), collagen (Col) and fine
fibrils (Fib). Some fibers (unlabelled arrows) that mingle with the collagen appear deeply scalloped
i n transverse sections; G , granules i n the elastic rncmbrane; F, process of a fibrocyte external to the
elastic membrane. 40,000.
Fig. 7 Segment of the arterial elastic membrane close to the arteriovenous junction. The outer
elastic lamina ( E l ) is disappearing, the inner zone of fine elastic fibers (el) becomes wider and extends
into the wall of the vein (cf. with figs 8-10). G, granule in the membrane; m, subendothelial muscle
cell; F, process of a fibrocy te. >: 20,000.
fine elastic fibers became wider and extended into the vein where it formed the
outer one half of its wall1 (figs. 8, 10).
The tunica media of the anastomotic
artery mainly consisted of smooth muscle
cells arranged in compact concentric layers (Tm in figs. 1, 2 ) . The basement membrane system of the musculature was well
developed. Some elastic fibers coursed between the muscle cells, but an external
elastic membrane was absent. The circular muscle cell layer ended about 1 0 0 p
short of the junction between the artery
and the vein thus exposing the modified
elastic membrane of the artery to the adventitia (asterisk in fig. 2, cf. with el in
fig. 8).
The tunica adventitia of the artery contained fibrocytes, some elastic fibers of irregular arrangement and loose collagen
bundles which supported a number of vasa
vasorum and fascicles of non-myelinated
The venous segment
The structure of the thin walled vein was
basically different from that of regular
veins. The tunica intima consisted of a
closed endothelial tube supported externally by a basement membrane of regular
appearance (End and BM in fig. 9). The
rest of the wall was characterized by a total absence of musculature and a near
absence of other cellular elements (figs. 8,
9, 10). The inner portion of the wall consisted of a fine mesh of matted elastic fibers
mingled with fascicles of collagen fibers
of varying orientation (el and Col in fig.
9). Towards the adventitia, the elastic fibers became coarser while the collagen
component disappeared. The outer layer
of the wall consisted of an elastic mesh
which was a direct continuation of the inner zone of the arterial elastic membrane.
Like the latter, it contained spherical granules (G in fig. 1 0 ) scattered among the
fiber fascicles.
Fig. 8 Arteriovenous junction (cf. with V in fig. 2). L, lumen; m, subendothelial smooth
muscle cells of the artery; el, modified elastic membrane continuous from the artery into the
vein (V). El, elastic fibers external to the vessel wall. ~4,000.
The nerve su p p ly
All nerves of the arteriovenous anastomosis were non-myelinated and were located in the adventitia of the arterial
segment. They never penetrated into the
tunica media. The subendothelial muscle
cell layer was devoid of nerves. The axons
were of the beaded variety. Their narrow
segments were closely enwrapped by the
Schwann sheath and usually showed few
morphologically defined axoplasmic components except for some fibrillar or tubular
elements. The enlarged segments of the
axons were partly covered by the Schwann
cell cytoplasm and partly exposed to the
intercellular space and the musculature of
the blood vessels. The axolemma of the exposed parts of the axons, however, showed
no apparent morphological specialization.
and its external aspect was covered with
the basement membrane of the nerve (figs.
11, 12, 13). Their axoplasm contained mitochondria, glycogen granules, and occasional vacuoles (figs. 11-13). In addition,
the axons contained accumulations of microvesicles. Over the proximal segment of
the anastomosis, such as shown in figure
1, some axons only contained agranular
vesicles that usually characterize cholinergic nerves (fig. 12). Others contained a
Figs. 9-10 Luminal and adventitial portions of the wall of the vein (cf. with V in fig. 8 ) . L,
lumen; End, endothelial cell; BM, endothelial basement membrane; Col, twisting bundles of collagen
fibers; el, bundles of fine elastic fibers; G, granule in the adventitial elastic mesh; Adv, adventitial surface of the vein. x 20,000.
mixture of agranular and small granular
vesicles (arrows in fig. 11) as encountered
in adrenergic nerves (Grillo, '66; Hokfelt,
'68). In the immediate vicinity of the arteriovenous junction, there were fewer
adventitial nerves. The fascicles were
smaller and usually were closely related to
the vasa vasorum of the artery (fig. 13).
The latter contained a layer of smooth
muscle cells around the periphery of their
endothelial tubes ( m in fig. 13). The axons
of the related nerves only contained accumulations of small agranular vesicles and
were exposed to the muscle cells (arrows in
fig. 13).
The arteriovenous anastomosis has a
typical fine morphology which is differsnt
from that of the regular arteries and veins
of the same caliber. Its most conspicuous
feature is the longitudinal smooth musculature which produces subendothelial
cushions i n the proximal segment of the
artery and expands into a thick uniform
layer before the artery joins the vein (figs.
1, 2 ) . According to Clara ('39), the longitudinal muscle cells undergo epithelioid
modification in certain kinds of anastomoses. Mark ('41) and Rossatti ('54) using
the optical microscope state that the anastomoses of the human nose contain epithelioid cells as defined by Clara, whereas
Temesrekasi ('69 1 has the opposite view.
Dawes and Prichard ('53) find that the
musculature of the anastomotic artery in
the nose of the cat and dog partly consists
of smooth muscle cells and partly of the
epithelioid type. In the present material,
the cells in question have the characteristics of smooth muscle fibers and cannot be
distinguished from the muscle cells of the
tunica media on a morphological basis
(figs. 3-5, 7, 8, cf. with m i n fig. 12).
However, histochemically the muscle cells
exhibit butyrocholinesterase activity not
observed in the musculature of the regular
nasal blood vessels (Cauna et al., '69).
According to Luckner ('55) the subendothelial cells also contain acetylcholine at
least in the glomus organ. The specialized
muscle cells may have other histochemical
properties that are not recognized morphologically.
The porosity of the endothelial basement
membrane is one of the characteristics of
the nasal blood vessels (Cauna and Hinderer, '69). As a result of this condition. the
subendothelial musculature of the vessels,
including that of the anastomosing artery
may readily be influenced by agents carried
i n the blood (fig. 3 ) . This finding may explain clinical and experimental observations that the nasal blood vessels are particularly sensitive to drugs introduced
through the blood stream (Sherman, '63;
Stovall and Jackson, '67). Experimental
studies also show that the arteriovenous
anastomoses are particularly sensitive to
changes in blood composition such as hypoxia (Luckner, '55) and variations in the
pH values (Walder, '52).
The elastic membrane separates the subendothelial musculature from the muscle
layer of the tunica media and from the
nerves that are located in the tunica adventitia (El in fig. 5 ) . The musculature of the
tunica media and the vasa vasorum of the
artery are probably controlled by the periarterial nerve plexus. Experimental and
clinical evidence suggests that the cholinergic fibers of the nasal blood vessels are
derived from the greater petrosal nerve and
the sphenopalatine ganglion, while the
adrenergic ones from the superior cervical
ganglion (Malcomson, '59). The occurrence of a dual nerve supply is confirmed
by the present morphological findings (figs.
11-13). There are no specialized contact
areas between the axons of the adventitial
nerves and the muscle cells. Therefore, the
nervous control is probably effected indirectly by active agents that are released
from the nerves into the perivascular space.
These would reach the muscle cells of the
tunica media by diffusion. The subendoFig. 11 Non-myelinated nerve cut transversely
from the adventitia of the artery shown in figure
1. The four axons contain mitochondria, vacuoles
(Vc), glycogen granules and two kinds of microvesicles. The majority of the latter appear agranular while others are granular (arrows). S ,
Schwann cell; bm, basement membrane of the
nerve. x 60,000.
Fig. 12 Part of a non-myelinated nerve from
the adventitia of the same artery as in figure 11.
The axon (Ax) is partly enwrapped by Schwann
cell ( S ) and partly exposed towards the muscle
cell ( m ) of the tunica media. The interval contains the basement membranes of the nerve and
the muscle cell (Bm), some fibers and a process
of a fibrocyte (F). The axoplasm of the ending is
filled with agranular vesicles, typical of cholinergic nerves. y 40,000.
Figures 11-12
Fig. 13 Part of a vas vasorum ( V ) and a related nerve from the adventitia of the arteriovenous
anastomosis (see fig. 2). The vessel possesses musculature ( m ) . The two axons (arrows) contain agranular vesicles. They are partly enwrapped by the Schwann cell ( S ) and partly exposed towards the
musculature of the vessel; bm, basement membrane, cut tangentially over the surface of the muscle
cell. x 40,000.
thelial musculature that is located on the
luminal aspect of the elastic membrane
would probably not be influenced by these
agents because of the distances involved
and because the elastic lamina may constitute an effective permeability barrier.
The nerves that are found in abundance
in the adventitia of the arterial segment
may not all be autonomic. Sensory nerves
proceed to the surface along with the arteries and veins. In the respiratory area
of the nose, these nerves are non-myelinated; they exhibit acetylcholinesterase
activity and contain accumulations of
agranular vesicles in their axoplasm
(Cauna et al., ’69). These apparently “cho-
linergic" sensory nerves may affect the activity of the nasal vessels including the
arteriovenous anastomoses by means of
axon reflexes (Cauna, "70). Experimental
studies with the anastomoses strongly suggest such a possibility (Grant, '29).
While the control mechanism of the arterial segment of the anastomosis appears
to be remarkably complex, none can be
recognized in the thin walled vein. The latter is devoid of musculature and its adventitia is devoid of nerves. The elastic wall
of the vein, however, appears to be well designed to receive blood at varying pressure
The author wishes to thank Dr. Kenneth
H. Hinderer for the supply of the samples
of the human nasal respiratory mucosa
and Mr. Charles Abbott for his aid with
the photographic work.
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nasal vascular bed and its nerve supply. In
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Studies of the vascular arrangements of the
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1969 Mikroskopischer Bau
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structure, respiratory, anastomosis, nerve, arteriovenous, supply, nasal, mucosal, human, fine
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