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Presence of fenestrated capillaries in the skin.

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Presence of Fenestrated Capillaries in the Skin
MITSUYA TAKADA AND SHIZUKO HATTORI
Department of Anatomy, Nagoya City University Medical School,
Mizuhoku, Nagoya, Japan 467
ABSTRACT
Capillaries of the skin have been thought to be of a nonfenestrated type according to studies of previous investigators. However, the
present study revealed that fenestrations exist in the endothelium of cutaneous
vessels. Capillary fenestrations are numerous in the human finger and the mouse
sole and are moderately frequent in the guinea pig sole and ear. In the skin of
the human chest, however, they are rarely encountered. Sometimes, endothelial
fenestrations are encountered in venules as well.
The structure of the vascular system
differs with the species of animal and the
tissue of distribution. Such vasculature
presents a structure characteristic for it
localized function. Blood vessels of the
skin differ from those of other tissues, in
that they not only supply nutrients to the
tissues but also perform important physiological functions such as adjustment of
blood pressure and regulation of body temperature. Because of this, a study of the
relationship between the structure and
function of cutaneous blood vessels was
undertaken. A reinvestigation of the ultrastructure of these vessels has yielded new
information and clarifies several points
concerning the nature of the endothelium.
OBSERVATIONS
Fenestrated capillaries are found in the
dermis of the human finger (fig. 1 ) and
chest (fig. 2 ) , the guinea pig sole and ear,
and the mouse sole (fig. 3 ) . They are numerous in the human finger and the mouse
sole and are of moderate frequency in the
guinea pig sole and ear. However, in the
human chest they are rarely encountered,
because the number of fenestrations is
small in this location (fig. 2). In all materials, fenestrated capillaries exist unrelated to the sebaceous and sweat glands,
and they are more frequently observed in
the papillary layer than in the reticular
layer. Especially, in the papillae of the
human finger (fig. 1) and mouse sole,
capillaries are observed to have numerous
endothelial fenestrations. Infrequently, enMATERIALS AND METHODS
dothelial fenestration are encountered in
Small pieces of the skin including epi- the venules up to 30 in diameter. The
dermis and dermis were removed from ( a ) ultrastructure of the fenestration in the
the palmar surface of the fmger of a 51 cutaneous vessels is similar to that in other
year old woman under local anesthesia (b) vessels reported before (Elfvin, '65; Luft,
the chest, in front of the sternum, of a '65; Palade and Bruns, '68; Rhodin, '62;
seven year old boy and a 29 year old wom- Takada, '70).
an under general anesthesia, (c) guinea
DISCUSSION
pig soles and ears and (d) mouse soles.
After fixation in 1% OsOl in Veronal aceCapillaries of the skin have been retate buffer, the tissue blocks were treated ported to be of a non-fenestrated type by
for two hours with 0.5% uranyl acetate in the studies of Bennett, Luft and Hampton
Veronal acetate buffer (Palade and Bruns, ('59), Odland ('61) and White and Claw'68). Ethanol was used for dehydration, son ('67). Moreover, in the review of
Epon 812 for embedding, lead citrate for Majno ('65) cutaneous capillaries were not
staining of thin sections and an Hitachi HU included in the group of fenestrated capil11D electron microscope for examination.
Received Oct. 13,'71. Accepted Jan. 31, '72.
ANAT.REC., 173: 213-220.
213
214
MITSUYA TAKADA AND SHIZUKO HATTORI
laries. However, our detailed observations
revealed that fenestrations exist in the endothelium of cutaneous vessels. On considering the reasons why existence of the
fenestrations has been overlooked by previous investigators, we note first that electron microscopic studies of cutaneous
capillaries are relatively few, compared
with those of other areas. The second is
that a small number of fenestrations
exist in the cutaneous capillaries except
for fingers and soles. In the materials examined in the present study, numerous
fenestrations were observed in the capillaries of fingers and soles, in which long
dermal papillae exist. This finding confirms Casley-Smith ('67) who also found
fenestrated blood capillaries in the rat
foot pads, during the study of lymphatics.
Besides, Rhodin ('68) reported the presence of fenestratsd capillaries in the hypodermis (muscle fascia of the rabbit thigh)
and Stehbens and Ludatscher ('68) noted
that the vessels of the senile angiomas in
the human trunk were lined by fenestrated
endothelium. The latter authors studied
angiomas on the assumption that fenestrations had never been observed in the endothelium of vessels related to the skin of
man or other mammals. Hibbs, Burch and
Phillips ('58) reported that capillaries in
the dermis near the sweat glands have
unusually thick endothelium, but this finding was subsequently revised by Matsuzawa and Kurosumi ('63) who found
fenestrated capillaries.
In conclusion, the present study reveals
that endothelial fenestrations exist in the
cutaneous capillaries which were referred
to as a non-fenestrated type. Perhaps the
presence of fenestrated capillaries in the
skin may be useful in clarifying the
physiological function of the cutaneous
vessels.
LITERATURE CITED
Bennett, H. S., J. H. Luft and J. C. Hampton
1959 Morphological classification of vertebrate blood capillaries. Am. J. Physiol., 196:
381-390.
Casley-Smith, J. R. 1967 Electron microscopical
observations on the dilated lymphatics in
oedematous regions and their collapse following hyaluronidase administration. Brit. J. Exp.
Pathol., 48: 680-688.
Elfvin, L.-G. 1965 The ultrastructure of the
capillary fenestrae i n the adrenal medulla of
the rat. J. Ultrastruct. Res., 12: 687-704.
Hibbs, R. G., G. E. Burch and J. H. Phillips 1958
The fine structure of the small blood vessels
of normal human dermis and subcutis. Am.
Heart J., 56: 662-670.
Luft, J. H. 1965 The ultrastructural basis of
capillary permeability. In: The Inflammatory
Process. B. W. Zweifach, L. Grant and R. T.
McCluskey, eds. Academic Press, New York,
PP. 121-157.
Majno, G. 1965 Ultrastructure of the vascular
membrane. In: Handbook of Physiology, Sect.
2. Circulation. W. F. Hamilton and P. Dow,
eds. AmeTican Physiology Society, Washington,
D. C., 3: 2293-2375.
Matsuzawa, T., and K. Kurosumi 1963 The
ultrastructure, morphogenesis and histochemistry of the sweat glands in the rat foot pads
as revealed bv electron microscoov.
_ .-6 . Electronmicroscopy, 12: 175-191.
Odland, G. F. 1961 The fine structure of
cutaneous capillaries. In: Advances i n Biology
Skin. Vol. 2. Blood Vessels and Circulation.
W. Montagna and R. E. Ellis, eds. Pergamon
Press, New York, pp. 57-70.
Palade, G . E., and R. R. Bruns 1968 Structural modulations of plasmalemmal vesicles.
J. Cell Biol., 37: 633-649.
Rhodin, J. A. G. 1962 The diaphragm of
capillary endothelial fenestrations. J. Ultrastruct. Res., 6: 171-185.
__ 1968 Ultrastructure of mammalian
venous capillaries, venules, and small collecting veins. J. Ultrastruct. Res., 25: 452-500.
Stehbens, W. E., and R. M. Ludatscher 1968
Fine structure of senile angiomas of human
skin. Angiology, 19: 581-592.
Takada, M. 1970 Fenestrated venules of the
large salivary glands. Anat. Rec., 166: 605-610.
White, J. G., and C. C. Clawson 1967 Blood
cells and blood vessels. In: Ultrastructure of
Normal and Abnormal Skin. A. S. Zelickson,
ed. Lea & Febiger, Philadelphia, pp. 261-303,
PLATES
PLATE 1
EXPLANATION OF FIGURES
216
1
A portion of a capillary in the papilla of the skin removed from the
palmar surface of the human finger. Several fenestrations (arrows)
are seen in the endothelium. A portion of a basal cell of the epidermis
( E ) is above. x 41,000.
2
A capillary in the dermis of the chest from a 29 year old woman.
Only one fenestration (arrow) is present. x 22,000.
FENESTRATED CAPILLARIES IN SKIN
Mitsuya Takada and Shizuko Hattori
PLATE 1
217
PLATE 2
EXPLANATION O F F I G U R E
3 Deep portion of the reticular layer of the mouse foot pad. In the wide
area of the connective tissue a capillary is seen. It has fenestrations
(arrows). At higher magnification (inset) three fenestrations are
closed by a diaphragm with a central knob. A portion of a lymphatic
vessel ( L ) is above and a nerve ( N ) below. x 10,000; inset, x 32,000.
218
FENESTRATED CAPILLARIES IN SKIN
Mitsuya Takada and Shizuko Hattori
PLATE 2
219
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