Download Veterinary Pathology Online

Veterinary Pathology Online
http://vet.sagepub.com/
Blood and Serous Cysts in the Atrioventricular Valves of the Bovine Heart
P. S. Marcato, C. Benazzi, G. Bettini, M. Masi, L. Della Salda, G. Sarli, G. Vecchi and A. Poli
Vet Pathol 1996 33: 14
DOI: 10.1177/030098589603300102
The online version of this article can be found at:
http://vet.sagepub.com/content/33/1/14
Published by:
http://www.sagepublications.com
On behalf of:
American College of Veterinary Pathologists, European College of Veterinary Pathologists, & the Japanese College of Veterinary
Pathologists.
Additional services and information for Veterinary Pathology Online can be found at:
Email Alerts: http://vet.sagepub.com/cgi/alerts
Subscriptions: http://vet.sagepub.com/subscriptions
Reprints: http://www.sagepub.com/journalsReprints.nav
Permissions: http://www.sagepub.com/journalsPermissions.nav
>> Version of Record - Jan 1, 1996
What is This?
Downloaded from vet.sagepub.com by guest on July 25, 2013
Vet Pathol33:14-21 (1996)
Blood and Serous Cysts in the Atrioventricular
Valves of the Bovine Heart
P. S. MARCATO,
C. BENAZZI,
G. BETTINI,
M. MASI,L. DELLA
SALDA,
G. SARLI,G. VECCHI,
AND A. POLI
Institute of Veterinary Pathology, University of Bologna, Bologna, Italy (PSM, CB, GB, LDS, GS);
Unita Sanitaria Locale 24, Budrio, Bologna, Italy (MM);
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia, Sezione di Bologna, Bologna, Italy (GV); and
Department of Animal Pathology, University of Pisa, Pisa, Italy (AP)
Abstract. A survey of 30,907 slaughterhouse cattle (5,984 calves, 15,937 young adult, 8,986 cows) was
carried out to determine the incidence of blood and serous cysts on atrioventricular valves. The cysts were
classified by their content (blood/serous fluid), location (mitral/tricuspid valve), and size. Cyst wall samples
were processed for histology, immunohistochemistry for factor VIII-related antigen, and transmission electron
microscopy. The content of some cysts was studied by electrophoresis and biochemical and microbiologic
methods. Older cows had a higher incidence (16.2%) than younger animals (1 1.5% in calves, 7.9% in steers,
6.4% in heifers), suggesting that the lesions may be acquired. Blood cysts were often present on both atrioventricular valves; serous cysts prevailed on the mitral valve. Cysts of both types were larger in older animals;
serous cysts were larger than the blood cysts. Histologically, blood cysts contained fresh blood, and serous cysts
were filled with a hyaline fluid devoid of cells, sterile, and biochemically similar to lymph. All the cysts were
lined with endothelium, but a positive immunostaining for the factor VIII-related antigen was appreciable only
in blood cysts. Ultrastructurally, the endothelium was composed of flat endothelial cells holding several cytoplasmic filaments, lying in blood cysts on a continuous and often laminated basal lamina with many cytoplasmic
projections. The results support the hypothesis that cysts of the atrioventricular valves derive from the dilation
of blood and lymphatic valvular vessels, do not regress with age, and are mainly the result of mechanical effects.
Key words: Atrioventricular valves; blood cysts; cattle; endothelial cells; factor VIII-related antigen; heart;
immunohistochemistry; ultrastructure; valvular cysts.
Blood cysts of the cardiac atrioventricular (AV)
valves, first described in humans in 18443 and subsequently in 1857,15have been frequently reported as
incidental necropsy findings in fetuses and infants under 6 months of age, with no pathologic relevance except for giant blood cysts, which may produce valvular
stenosis requiring surgical treatment.4. 4,
Blood cysts of the AV valves have been described
as common congenital lesions that spontaneously tend
t o regress with age in dogs, pigs, and
but
only a few studies have dealt with a significant number
of animal^.^^,^^
Here, we report a high frequency of valvular cysts
in both young and adult cattle that was recorded during
an abattoir survey on bovine cardiac pathology. Besides blood cysts, another less common type of valvular cyst containing a yellow fluid material was observed and referred t o as a serous cyst. The morphology
and content of the two types of cysts were investigated
by means of histologic, immunohistochemical, electrophoretic, microbiologic, and ultramicroscopic techniques.
Material and Methods
Hearts from 30,907 cattle slaughtered from June to October 1991 in a private abattoir near Bologna, Italy, were
examined to investigate the prevalence of valvular cysts. The
animals examined were 5,984 calves (4-5 months of age,
Holstein-Friesian males), 15,937 young adults (14-1 5 months
of age, Holstein-Friesian and Limousine, 14,024 steers and
1,913 heifers), and 8,986 cows (5-8 years of age, HolsteinFriesian).
The hearts were longitudinally sectioned, and the atrioventricular valves were carefully examined for the presence
of cysts, which were classified according to their content as
blood or serous cysts. When both types of cysts were present
in the same heart, the prevailing type only was scored. In a
series of 4 12 affected hearts, the valvular cysts were counted
and measured and their anatomical location (tricuspid or
mitral valve) was recorded.
For the histologic examination, representative samples from
affected valves (20 blood cysts and 20 serous cysts for each
age class) were fixed in 10% buffered formalin and embedded
in paraffin. Five-micrometer-thick serial sections were stained
with hematoxylin and eosin, Orcein-Van Gieson’s stain for
elastic and collagen fibers, Gomori’s stain for reticulin, and
14
Downloaded from vet.sagepub.com by guest on July 25, 2013
Valvular Cysts in Cattle
Vet Pathol 33:1, 1996
15
Table 1. Prevalence of cysts of the atrioventricular valves in 30,907 cattle.
Prevalence
Blood Cysts
Serous Cysts
Age Class
n
No. Cysts
Calves
Young adults
Steers
Heifers
cows
5,984
15,937
14,024
1,913
8,986
687
1,227
1,104
123
1,454
11.48
7.70
7.87
6.43
16.18
408
544
489
55
624
6.82
3.41
3.49
2.88
6.94
279
683
615
68
830
4.66
4.29
4.39
3.55
9.24
Total
30,907
3,368
10.90
1,576
5.10
1,792
5.80
(O4
Perk’ stain for hemosiderh and with the periodic acidachiff
(PAS) reaction.
For immunohistochemistry, sections from 20 specimens
(10 blood cysts and 10 serous cysts) were dewaxed and rehydrated, and endogenous peroxidase was blocked with 3%
hydrogen peroxide for 60 minutes at room temperature (RT).
The sections were then incubated with Protease XIV (Sigma,
St. Louis, MO) 0.05% in Tris buffer for 5 minutes at 37 C.
After preincubating for 30 minutes with 1 : 20 normal goat
serum (Dakopatts, Copenhagen, Denmark), the sections were
allowed to react with the primary antibody, rabbit anti-human Von Willebrand factor (Dakopatts) diluted 1 : 3,000
overnight at 4 C. Biotinylated goat anti-rabbit immunoglobulin (BIO SPA, Milan, Italy; diluted 1 : 100) followed by peroxidase streptavidin (BIO SPA, diluted 1 :250) were used as
secondary and tertiary staining reagents, respectively, at RT
for 30 minutes. Diaminobenzidine (Sigma) (0.04%, 7 minutes) was used as chromogen, and the sections were then
counterstained with Papanicolau hematoxylin.
For transmission electron microscopy, valvular cysts samples (three blood cysts and three serous cysts for each age
class) were excised from the hearts about 30 minutes after
slaughter. Specimens 1-3 mm thick were fixed for 3 hours
in 5% glutaraldehyde in 0.1 M cacodylate buffer, pH 7.2,
rinsed in the same buffer, and postfixed for 1 hour in 1%
osmium tetroxide in 0.1 M cacodylate buffer, pH 7.2. After
dehydration in a graded sequence of alcohols, the specimens
were then embedded in Durcupan AcM resin. Semithin sections were stained for light microscopy with toluidine blue,
and ultrathin sections were stained with uranyl acetate and
lead citrate and examined in a Philips CMlO transmission
electron microscope.
Protein concentration of the serous cyst content and of the
blood serum from two calves, two steers, one heifer, and two
cows was quantified using a commercial assay (Bio Rad,
Richmond, CA), and protein analysis was performed using
sodium dodecyl sulfate-polyacrylamide gel electrophoresis as
previously described. I Gels were stained using Coomassie
bnllant blue R-250 and analyzed by densitometric scanning
(Model 620 Densitometer, Bio Rad). Molecular weights of
single bands were established by comparison with prestained
low-molecular-weight markers (Bio Rad).
Chloride concentrations of the same samples of blood serum and serous cyst content were determined by a Stat Profile
4 Analyser (Nova Biomedical, Waltham, MA).
For microbiologic examination, 0.01 ml from cyst fluid
samples (nine blood cysts and nine serous cysts, three samples
No.
No.
%
YO
for each age class) were cultured on the following solid media:
blood agar, Gassner medium, brain-heart infusion, Yoder
agar, and Protease-3-agar and on the following fluid media:
Yoder broth, SAT medium, and tyoglycolate broth. Cultures
were incubated at 37 C in normal atmosphere and in an
atmosphere containing 12% CO,. Solid media were incubated for 96 hours and examined at 24-hour intervals. Liquid
media were examined every 24 hours, and after 48 hours of
incubation 0.0 1-ml samples were transferred to solid media
and incubated as indicated above.
Results
T h e valvular cysts prevalence in the 30,907 exam-
ined cattle is listed in Table 1.
Macroscopic findings
Macroscopically, the cysts were always sessile and
roundish or oval and protruding above the atrial surface of the valvular leaflets (Figs. 1, 2). They were 1
mm to 3 cm in diameter. The serous cysts were significantly larger than the blood cysts by analyses of
variance (ANOVA; P < 0.001), and the cysts on the
mitral valve were larger than those on the tricuspid (P
< 0.001). Both types of cysts showed a tendency to
enlarge with advancing age (Table 2).
Fig. 1. Mitral valve, heart; cow. A large blood cyst (arrow) (diameter = 1.5 cm) and a serous cyst (arrowhead) (diameter = 1.0 cm) are close to the valve base of the two
valvular leaflets.
Downloaded from vet.sagepub.com by guest on July 25, 2013
Marcato, Benazzi, Bettini, Masi, Della Salda, Sarli, Vecchi, and Poli
16
Vet Pathol 33:1, 1996
Histologic findings
Fig. 2. Mitral valve, heart; cow. A large serous cyst (diameter = 1.5 cm) is lying near the valve base.
Blood cysts were mostly unilocular and frequently
multiple (Table 3) (up to seven on the same valve). In
some cases, several blood cysts were grouped together
so that the lesion had a multilocular appearance.
Serous cysts were unilocular and usually single (Table 3). When the same valve exhibited more than one
serous cyst (maximum of three), these were generally
located on separate leaflets. The serous cysts were generally close to the base of the valvular leaflet (Fig. 2),
but the largest ones showed a tendency to invade the
whole surface of the leaflet.
Blood cysts were most frequently present on both
mitral and tricuspid valves except in cows, where they
prevailed on the tricuspid valve; serous cysts were preferably located on the mitral valve in all three age classes
(Table 4). A serous cyst was also found on a chordu
tendinae of a papillary muscle of the mitral valve in
one cow, and a second cyst arose from the endocardium of the left ventricular wall in another cow.
Blood and serous cysts were often associated in the
same valve (Fig. l), and in some hearts the coexistence
of blood and serous cysts was observed in both AV
valves.
Some microscopic differences were found between
blood and serous cysts, independent of the age of the
animal. The histologic description therefore applies to
all three age classes.
Cysts were located in the spongiosa of the valves,
which is the looser part of the leaflet. Both types of
cysts were internally lined by typical endothelium, lying on an inconspicuous PAS-positive basement membrane.
Blood cysts contained intact red blood cells and leukocytes. The wall was mainly composed of several irregular layers of elastic fibers intermingled with some
dense collagen and few reticular fibers. Small blood
vessels and multilocular spaces of different sizes were
present in the wall or close to the cysts, near the valve
base. Serial sections revealed dilated blood vessels in
direct connection with the blood cyst lumina. No ironpositive macrophages were found near blood cysts.
Serous cysts contained a homogenous acidophilic
and weakly PAS-positive material, generally devoid of
cells except for occasional macrophages containing
granules of a yellowish PAS-positive and iron-negative
pigment. The wall of the serous cyst was always thinner
than that of the blood cyst and lacked dense collagen.
No blood vessels were found in the wall. However, a
few small endothelium-lined channels were observed,
connected with the lumen and directed toward the valve
base.
No direct connection was observed between cyst lumina and the ventricular cavities.
Immunohistochemical findings
The endothelium of blood cysts showed a constant
positive staining for factor VIII-related antigen that
was usually as intense as the staining in the blood
vessels of the same section, except that the larger blood
cysts showed a weaker and focally interrupted positive
staining.
The endothelium of serous cysts was always negative
for the antigen.
Table 2. Diameter (mm) of blood and serous cysts of the atrioventricular valves in 4 12 cattle.
Mitral Valve
Age Class
n
Blood Cysts
P
Mean
Range
P
<0.05
5.0
7.5
10.8
2-15
2-20
1-35
<0.001
<0.01
<0.001
Mean Range
Calves*
Steers/heiferst
Cows§
79 2.7
140 3.5
193 4.0
1-10
1-15
1-20
Tricuspid Valve
Blood Cysts
Serous Cysts
Serous Cysts
NS$
<0.001
Mean Range
2.4
2.9
2.9
* P values for ANOVA of calves versus steers and heifers.
*8
t P values for ANOVA of steers and heifers versus cows.
NS = not significant.
P value for ANOVA of calves versus cows.
Downloaded from vet.sagepub.com by guest on July 25, 2013
1-8
1-10
1-8
P
<0.01
NS
<0.05
Mean Range
3.5
7.0
9.6
2-5
3-15
2-30
P
<0.05
NS
<0.05
Valvular Cysts in Cattle
Vet Pathol 33:1, 1996
17
Table 3. Number of cysts present on the atrioventricular valve leaflets of 412 cattle.
Mitral Valve
n
Age Class
Calves
Steers and heifers
cows
79
140
193
Blood Cysts
Tricuspid Valve
Serous Cysts
Blood Cysts
Serous Cysts
Mean
Range
Mean
Range
Mean
Range
Mean
2.1
1.5
1.3
1-6
1-4
1-3
1.4
1.2
2-4
1-3
1-3
2.1
1-5
1-7
1.2
1.1
1.2
2.1
1.5
1-7
1.1
Range
1-2
1-2
1-2
mon in calves, especially newborns. Previous reports
have
stated that these cysts do not usually persist for
Blood cysts were internally lined by flat endothelial
more
than a few months, except in rare cases in which
cells having ovoid or convoluted nuclei with irregular
they
may
enlarge and persist for more than 1 year,
borders and scarce cytoplasm containing several filaduring
which
time their content changes into a serous
ments, mitochondria, ribosomes, and micropinocyfluid.6,20
totic vesicles (Fig. 3). The cell boundaries showed nuIn one study,2cysts of the AV valves, up to pea-size
merous cytoplasmic projections that were fingerlike at
and
filled with blood or serous-watery fluid, were said
the luminal face and rootlike at the abluminal face.
to
affect
up to 75% of calves and to regress during the
The endothelial cells lay on a continuous basal lamina
life
time
by resorption and organization phenomena.
with frequent aspects of duplication and lamination.
The
results
of our study contrast these widespread
The wall of the blood cysts was composed of elastic
ideas:
1)
blood
cysts and serous cysts may be regarded
and collagen fibrils and fibroblasts in an amorphous
as
separate
entities;
and 2) cysts of the AV valves do
matrix containing proteoglycan particles.
not
regress
with
age,
and
their incidence and dimension
The endothelial cells lining serous cysts (Fig. 4)were
are
significantly
increased
in older animals.
similar to those of the blood cysts, although their cyBlood
cysts
affected
both
valves, were small, and
toplasmic filaments were far more numerous and arcontained
fresh
blood.
Their
endothelium was imranged parallel to the basal lamina or encircling the
munohistochemically
positive
for
the factor VIII-renucleus. Adjacent endothelial cells were closely conlated
antigen,
and
the
wide
lamination
of the basal
nected by extensive overlapping of fingerlike cytolamina
was
as
described
in
blood
vessels
end~thelia,~
plasmic projections, and rootlike processes projecting
into the underlying tissue were rare. The basal lamina both factors indicative of their blood vessel origin. l 7
was single layered or slightly duplicated, but it never The observed focal discontinuities of the immunoshowed any lamination as seen in blood cysts. The positivity may be the result of the dilation of the larger
serous cyst wall was composed of loose connective cysts; as previously noted," the positivity for this antissue rich in proteoglycans, with fibroblasts and scat- tigen becomes weaker as the caliber of vessels increases.
tered elastic and rare collagen fibrils.
Serous cysts were larger and usually solitary and more
Other investigations
frequently affected the mitral valve. The lack of enThe results of the biochemical and electrophoretic dothelial reaction to factor VIII-related antigen, the
analyses of the serous cyst fluid and blood serum are extensive overlapping of the fingerlike projections of
adjacent cells, and the numerous perinuclear filaments
shown in Table 5.
in
the endothelial cells are regarded as distinctive feaMicrobiologic tests were negative for both types of
tures
of lymph vessel^.^^,'^
cysts.
Electrophoresis and biochemical analyses showed an
Discussion
analogy of components between serous cyst fluid and
Hematocysts of the AV valves, up to 1 cm in di- blood serum. Nevertheless, the cyst fluid contained a
ameter and sometimes multiple, are considered com- significantly (P = 0.0002) lower concentration of total
Ultrastructural findings
Table 4. Anatomical location of the valvular cysts of 4 12 cattle.
Age Class
Calves
Steers and heifers
cows
n
79
140
193
Blood Cysts
Serous Cysts
Tricuspid
Both
Mitral
Tricuspid
15 (21%)
41 (57%)
16 (22%)
2 (6%)
10 ( 14%)
13 (13%)
37 (33%)
63 (46%)
56 (50%)
36 (26%)
20 (18%)
39 (28%)
Downloaded from vet.sagepub.com by guest on July 25, 2013
Both
3 (10%)
5 (7%)
12 (12%)
Mitral
26 (84%)
56 (79%)
78 (76%)
18
Marcato, Benazzi, Bettini, Masi, Della Salda, Sarli, Vecchi, and Poli
Vet Pathol 33:1, 1996
Fig. 3. Transmission electron micrograph. Mitral valve, heart; steer. The endothelial cells (E) lining the blood cyst lie
on a thick and multilayered basal lamina (BL), pierced by rootlike cytoplasmic projections (arrows). Uranyl acetate-lead
citrate. Bar = 1 Mm.
proteins, with different proportions of albumin and
globulin, and a slightly (P = 0.1) higher amount of
chloride. These differences indicate that the serous cyst
content is similar to lymph.I6x2l
Several hypotheses have been formulated to explain
the mechanism of valvular blood cyst formation in
humans: 1) hematomas, 2) angiomas, 3) ventricular
endothelial infoldings of the valve leaflet bulged into
the atrium from the pressure gradient during the valve
closure and producing valvular diverticula, and 4) ectasia or dilation of blood vessels.
Cyst morphology excludes a traumatic or neoplastic
genesis. The third hypothesis assumes the existence of
connections between the cyst lumina and the ventricles
via small endothelium-lined channels,26but these connections have not been observed in this or in
studies.
Our results support the fourth hypothesis, as recently
proposed for canine blood valvular
and suggest
that bovine blood and serous cysts of the AV valves
may originate from the dilation of blood and lymph
vessels, respectively. Cysts of the AV valves morphologically equivalent to these bovine serous cysts have
been observed in slaughtered pigs and were empirically
regarded as distended lymphatic vessels.8JoJs
The existence of blood and lymphatic vessels in the
AV valves was at one time c o n t r o ~ e r s i abut
l ~ ~has
~ been
definitely proven in both humans and animals.I2 In
cattle, a particularly profuse valvular capillary plexus,
which extends to the closing edges of the AV valves,
has been described23and may be considered a predisposing factor for the high incidence of valvular cysts
in this species. Furthermore, a ventricular subendocardial network of small blood and lymph vessels that
drain into branches ascending the papillary muscles
and chordae tendinae has been described in the hearts
of pigs, dogs, sheep, cattle, and h ~ m a n s . The
~ , ~two
~
atypical serous cysts observed in a chorda tendinae and
in the left ventricular wall of two cows in this study
were located along the course of lymph vessels.
The higher frequency of larger valvular cysts in cows
than in young cattle contrasts with the general opinion
Downloaded from vet.sagepub.com by guest on July 25, 2013
Valvular Cysts in Cattle
Vet Pathol 33:1, 1996
19
Fig. 4. Transmission electron micrograph. Mitral valve, heart; steer. There is extensive overlapping (arrow) of the
cytoplasmic projections of two adjacent endothelial cell (E) in a serous cyst. Uranyl acetate-lead citrate. Bar = 1 pm.
that valvular cysts are congenital lesions that regress
during the first year of life. Our observations support
the hypothesis that valvular cysts persist and enlarge
during the entire life time and that they may also be
acquired later in life. Likewise, low-degree congenital
ectasias of vessels might become grossly observable
only after age-related enlargement.
Etiologic factors leading to blood cyst formation are
unknown. It has been supposed that mechanical effects,
such as an increase in tension, friction, and impact,
can trigger the enlargement of valvular blood vessels
in a sort of valvular telangiectasis with subsequent cyst
formation.24
Sex does not appear to play any role in the development of valvular cysts. The fact that all the affected
calves were male and all the adults were cows was only
a sampling artifact. The group of young adults, formed
by male and female cattle, showed a similar incidence
of cysts in both sexes.
In addition to the progressive enlargement of the
valvular cysts, advancing age seems to correlate with
a decrease in the number of blood cysts and an increase
Table 5. Electrophoretic and biochemical analysis of the fluid contained in the serous cysts and of the homologous blood
serum.
Sample
Total protein
Wdl)
Mean
Serous cyst content
Blood serum
Range
2.9
2.2-4.3
6.0
5.1-7.0
P*
0.0002
* t-test for paired samples.
Albumin
Wdl)
Mean
Range
1.35 0.85-2.9
1.77 1.09-2.38
0.08
Immunoglobulin
(g/dl)
Mean
Range
0.06
0.04-0.1
0.36
0.25-0.59
0.0009
Downloaded from vet.sagepub.com by guest on July 25, 2013
Hemoglobin
(g/W
Mean
Range
0.007
0.36
0.02
0-0.04
0.13-0.8
Chloride
(mEq/liter)
Mean
Range
123.8 120-129
120.8 116-124
0.1
20
Marcato, Benazzi, Bettini, Masi, Della Salda, Sarli, Vecchi, and Poli
-
Specific bovine predisposition:
- profuse valvular
capillary plexus
- ossification of the
anulus fibrosus
Fig. 5. Suggested pathogenetic mechanism for the valvular cyst formation in cattle.
in the number of serous cysts. A change from blood
to serous contentZodoes not seem likely, however, because blood and serous cysts have a different predilection for mitral and tricuspid valves and a different
anatomical structure. Moreover, in this large sample
of animals no form of transition between blood and
serous cysts was observed.
The predilection of the serous cysts for the mitral
valve could be related t o a lower capacity of the lymphatics, which have thinner walls than hematic vessels,
to withstand the dilation consequent from the systolic
pressure gradient, which is stronger in the left ventricle
than in the right one. This explanation may also suffice
for the larger dimension of the cysts located on the
mitral valve.
At the atrial surface of the tricuspid and mitral valves,
there are lymph capillaries that extend from the free
margins of the cusps t o the anulusfibrosus of each
valve, where they drain into a channel passing through
the myocardium and joining the subepicardial duct of
the atrioventricular S U ~ C U S . ~
The bovine physiologic age-related ossification of
the anulus Jibrosus may hinder the lymph outflow
through the transmyocardial channels and facilitate the
dilation of the valvular lymph vessels, which may thus
explain the high frequency and large dimensions of
serous cysts in adult cattle.
Other age-related predisposing factors (Fig. 5 ) would
be the progressive obstruction and diminution of the
valvular blood and lymph vessels9Jz and the progressive loosening of the spongiosa stratum of the AV
valves.'
References
1 Boyd TAB: Blood cysts on the heart valves of infants.
Am J Pathol 25757-759, 1949
Vet Pathol 33:1, 1996
2 Drommer W: Kreislauforgane. In: Pathologie der Haustiere, ed. Schulz LC, TeilI, p. 25. Fischer, Jena, Germany,
1991
3 Elsasser C: Bericht iiber die Ereignisse in der Gebaranstalt des Catherinen-Hospitals im Jahre 1844. Med
Correspondenzblatt 14:297, 1844
4 Gallucci V, Stritoni P, Fasoli G, Thiene G: Giant blood
cyst of tricuspid valve. Successful excision in an infant.
Br Heart J 38:990-992, 1976
5 Ghadially FN: Ultrastructural Pathology of the Cell and
Matrix, 3rd ed., vol. 2, pp. 1060-1063. Buttenvorths,
London, England, 1988
6 Gopal T, Leipold HW, Dennis SM: Congenital cardiac
defects in calves. Am J Vet Res 47:1120-1121, 1986
7 Gross L, Kugel MA: Topographic anatomy and histology of the valves in the human heart. Am J Pathol 7:
445-473, 1931
8 Gupta PP: Cysts in the cardiac valves of swine. Indian
Vet J 46358-560, 1969
9 Johnson RA, Blake TM: Lymphatics of the heart. Circulation 33: 137-142, 1966
10 Jones JET: Observations on endocardia1 lesions in pigs.
Res Vet Sci 28:281-290, 1980
11 Laemmli U K Clevage of structural proteins during the
assembly of the head of bacteriophages T4. Nature 227:
680-685, 1970
12 Lautsch EV: Functional morphology of heart valves.
Methods Achiev Exp Pathol 5214-237, 197 1
13 Leak LV: Lymphatics. In: Blood Vessels and Lymphatics in Organ Systems, ed. Abrams DI 'and Dobrin
PB, pp. 135-153. Academic Press, Orlando, FL, 1984
14 Leatherman L, Leachman RD, Hallman GL, Cooley DA:
Cyst of the mitral valve. Am J Cardiol21:428-430, 1968
15 Luschka H: Die Blutergiisse in Gewebe der Herzklappen. Virchows Arch Pathol Anat 11:144-149, 1857
16 Miller AJ: Lymphatic system. In: Blood Vessels and
Lymphatics in Organ Systems, ed. Abrams DI and Dobrin PB, pp. 348-355. Academic Press, Orlando, FL, 1984
17 Mukai K, Rosai J, Burgdorf WHC: Localization of factor
VIII-related antigen in vascular endothelial cells using
an immunoperoxidase method. Am J Surg Pathol4:273276, 1980
18 Negro M, Guarda F Contributo all0 studio della patologia endocardica in suini regolarmente macellati. Selez Veter 30(1):235-248, 1989
19 Pasaoglu I, Dogan R, Oram A, Ozyilmaz F, Bozer Y :
Giant blood cyst of the left ventricle. Jpn Heart J 32:
147-151, 1991
20 Robinson WF, Maxie MG: The cardiovascular system.
In: Pathology of Domestic Animals, ed. Jubb KVF, Kennedy PC, and Palmer N, 3rd ed., vol. 3, p. 1 1. Academic
Press, Orlando, FL, 1985
21 Rusznyak I, Foldi M, Szabo G: Lymphologie, 2nd ed.,
pp. 359-375. Fischer, Stuttgart, Germany, 1969
22 Smith RB, Taylor IM: Blood cysts of the cardiac valves
of calves and cattle. Cardiovasc Res 5: 132-1 35, 1971
23 Smith RB, Taylor IM: Vascularization of atrioventricular and semilunar valves in cattle, pigs, and sheep. Cardiovasc Res 5: 194-200, 197l
24 Takeda T, Makita T, Nakamura N, Kimizuka G: Mor-
Downloaded from vet.sagepub.com by guest on July 25, 2013
Vet Path01 331, 1996
Valvular Cysts in Cattle
phologic aspects and morphogenesis of blood cysts on
canine cardiac valves. Vet Path01 28: 16-2 1, 199 1
25 Van Vleet JF, Ferrans VJ: Cardiovascular system. In:
Special Veterinary Pathology, ed. Thomson RG, p. 3 15.
Decker, Toronto, OW, Canada, 1988
21
26 Zimmerman KG, Paplanus SH, Dong S , Nagle RB: Congenital blood cysts of the heart valves. Hum Path01 14:
699-703, 1983
Request reprints from Prof. P. S. Marcato, Istituto di Patologia Generale e Anatomia Patologica Veterinaria, Via Tolara
di Sopra 50,I-40064,
Ozzano Emilia, Bologna (Italy).
Downloaded from vet.sagepub.com by guest on July 25, 2013