Download Congenital Heart Diseases in Swine

Vet. Pathol. 19: 676-686 (1982)
Congenital Heart Diseases in Swine
F. S. Hsu and S. J. Du
Department of Veterinary Medicine, Animal Industry Research Institute, TSC, Chunan,
Taiwan, and Department of Veterinary Pathology, Pig Research Institute of Taiwan,
Chunan, Taiwan, R.O.C.
Abstract. One hundred twenty-two congenital cardiac anomalies were diagnosed in 83 pigs
(4.35%) during necropsies of 1906 pigs from one day to four years of age during an 1 1-month
period.
The incidence of cardiac malformation was highest at 29 to 56 days of age. Of the 83 pigs
with cardiac anomalies, 47 (56%) were male and 36 (44%) were female, and of these, 15 (18%)
were purebred and 68 (82%) were crossbred pigs. Of the 15 purebred pigs with cardiac
malformation, there were seven Landrace pigs, four Large White pigs, three Duroc Jersey
pigs, and one Yorkshire pig; whereas 94% of the 68 crossbred pigs were crossbred among
Landrace, Duroc Jersey, and Large White.
The 122 cardiac anomalies found in the 83 pigs were: dysplasia of the tricuspid valve in 42
pigs, atrial septal defect in 31 pigs, subaortic stenosis in 22 pigs, ventricular septal defect in
nine pigs, persistent common atrioventricular canal in eight pigs, malformation of the
moderator band in seven pigs, persistent vena cava in one pig, persistent truncus arteriosus in
one pig, and pulmonary stenosis in one pig.
The pathological features of the anomalies in swine were similar to those described in small
animals and in man. The findings indicate that spontaneous porcine cardiac anomalies might
provide models for cardiovascular investigators to study the etiology and pathogenesis of
congenital heart diseases in man and other mammals.
Congenital heart diseases have been studied extensively in man and small animals,
but not in swine. Subaortic stenosis [6] and patent ductus arteriosus [ 111 are common
in pigs. In one study, seven (14.6%) of 48 pigs that were stillborn or died within two
weeks after birth were found to have congenital anomalies [20]. Eight cases (0.5%) of
cardiac malformation (dysplasia of the tricuspid valve in six pigs and persistent
common atrioventricular canal in two pigs) were recognized in necropsies of 1643
pigs 8 weeks to 3.5 years of age [23]. No pigs under 56 days of age were examined.
This study describes cardiac anomalies found on necropsy of 1906 pigs examined
in the Department of Veterinary Medicine, Animal Industry Research Institute,
Taiwan Sugar Corporation, ROC.
616
Congenital Heart Diseases in Swine
611
Materials and Methods
A total of 1906 pigs that died from disease were necropsied from 1 July 1978 to 30 April
1979. They were collected from a pig farm of the Animal Industry Research Institute, Taiwan
Sugar Corporation, Chunan, Taiwan, Republic of China. The study farm produces 70,000
hogs for market annually. The pigs from one day to four years of age were purebred or
crossbred. The crossbred pigs had two to four of the following breeds in their genetic
background: Landrace, Duroc Jersey, Yorkshire, Large White, and Minnesota.
At necropsy, the body weight of each carcass was recorded. The heart and 1.5 cm of the
aorta and major arteries were removed and examined. The right ventricle was opened through
the pulmonic valve (outflow tract) down to the apex. The left ventricle was opened from the
apex through the aorta and inflow tract. The thickness of the ventricular wall was measured
at the posterior left ventricular free wall, directly behind the midpoint of the posterior mitral
valve leaflet; the ventricular septum was measured in the area of maximal thickness, usually
about one-third to one-half the distance between the base of the aortic valve and the left
ventricular apex, and the right ventricular wall was measured near the tricuspid valve annulus.
In measuring ventricular wall thickness, we avoided the trabeculae or papillary muscles. The
entire heart was fixed in neutral 10% formalin and weighed 24 hours after fixation.
Specimens of myocardium were taken from the areas mentioned above, from lesions in the
left ventricular outflow tract, and from atrioventricular valves and moderator bands. The
specimens were embedded in paraffin, sectioned at 6 pm, and stained with hematoxylin and
eosin (HE), Masson trichrome, and periodic acid-Schiff.
The 1906 necropsied pigs were divided into five groups based on age: birth to 28 days
(suckling period), 29 to 56 days (nursing period), 57 to 110 days (growing period), 11 1 to 180
days (finishing period), and over 181 days (mature period).
A statistical analysis was done on relative heart weight and ratio of the thickness of
ventricular septa to left ventricular wall using a least significant difference procedure.
Results
Of the 1906 pigs examined during the 11-month period of study, 83 (4.35%) had
congenital heart diseases.
Age, sex, and breed distribution of the 83 affected pigs and the 1906 necropsied
pigs is found in table I. The majority (70%) of the affected pigs were less than 110
days old. Of the 83 pigs with cardiac anomalies, 47 (56%) were male and 36 (44%)
were female, and of these, 15 (18%) were purebred and 68 (82%) were crossbred pigs.
The pigs with congenital anomalies were poorly developed and had dyspnea,
lethargy, and anorexia. Often, these pigs died suddenly.
The types and frequency of diagnosed congenital heart disease are given in table
11.
Dysplasia of the tricuspid valve, diagnosed in 42 pigs, was the most common
cardiac anomaly. Of the 42 pigs, 33 (79%) had single anomalies. These 33 pigs were
from 18 days to 3.5 years of age, with most 29 to 56 days of age. Seventeen of the 33
affected pigs were males.
In the 33 pigs with dysplasia of tricuspid valve, relative heart weight, mean
thickness of ventricular free wall and septum, and ratio of ventricular septum to the
thickness of the ventricular free wall did not differ significantly from those pigs with
a normal heart.
Hsu and Du
678
Table I. Age, sex, and breed distribution of 1906 pigs studied
Age
Under 28 days
29 to 56 days
57 to 110 days
1 11 to 180 days
Over 180 days
Sex
Male
Female
Breed
Pure breed
Landrace
Large White
Duroc Jersey
Yorkshire
Cross breed
Cross breeds of Landrace,
Duroc Jersey, and Large
White
Pigs with
congenital
disease (%)
Tota.I pigs
necrop sied (%)
15.7
28.9
26.5
16.9
12.0
27.0
12.0
21.0
29.0
11.0
56.0
44.0
54.0
46.0
18.0
8.0
5.0
4.0
1.o
16.0
5.0
5.0
5.0
82.0
84.0
1.0
Table 11. Congenital cardiac malformations in 83 pigs*
Malformation
Number of
abnormalities
Dysplasia of the tricuspid valve
Atrial septal defect
Subaortic stenosis
Ventricular septal defect
Persistent common atrioventricular canal
Malformation of moderator band
Persistent cranial vena cava
Persistent truncus arteriosus
Pulmonary stenosis
Total
42
31
22
9
8
7
1
1
I
122
Percent
34.0
25.0
18.0
7.0
7.0
6.0
1.o
1.o
1.o
* A total of 1906 pigs were examined.
The morphological features (fig. 1) of the dysplasia of tricuspid valve included:
irregular thickening of the leaflets; attachment of the deformed leaflets to the
ventricular wall; absent or short, stout, fused chordae tendineae; abnormal insertion
of the deformed lateral leaflet into the papillary muscle; hypertrophy of the papillary
muscle; and enlargement of the right atrium and ventricle. Occasionally, the lateral
leaflet was nodular and contained clefts and multiple small fenestrations.
Additional cardiac anomalies in the affected pigs included five atrial septal defects
and four ventricular septal defects.
Congenital Heart Diseases in Swine
619
Fig. 1: Right side of heart from 22-day-old pig with dysplasia of the tricuspid valve.
Adhesion of anterior leaflet to fused moderator band (m) and papillary muscle (p); adhesion
of the thickened septal leaflet (s) to the septum, and insertion of the lateral leaflet into the
fused papillary muscle.
Fig. 2 Right side of heart from 76-day-old pig with atrial septal defect (arrow).
Fig. 3: Visceral organs from 76-day-old pig with atrial septal defect. Extensive dilatation of
heart with severe passive congestion of liver.
Fig. 4 Left side of heart from four-month-old pig with moderate subaortic stenosis. Fibrous
ridge (arrow) encircling ventricular outflow tract.
Atrial septal defect was diagnosed in 3 1 pigs, and 11 of these (35%) were single
anomalies. These 1 1 pigs ranged from five to 223 days of age; six of them were males.
The relative heart weight (8.27 f 5.73 gm/kg) in the 11 affected pigs was increased,
but was not significantly different from pigs with a normal heart (table 111).
The atrial septal defects varied in size from 3 to 9 mm and were found in the
dorsal and middle portions of the interatrial septum (fig. 2). The heart was enlarged
in all pigs and various degrees of passive congestion of visceral organs (fig. 3) were
observed.
The anomalies were accompanied by ventricular septal defect in seven pigs,
Hsu and Du
680
Table 111. Relative heart weight and cardiac muscle thickness in normal and affected pigs
Number
Normal3
TD
ASD
SAS
VSD
A-V canal
MMB
PTA
400
33
11
14
9
8
7
1
Relative
heart
weight'
6.28 f 3.18"
6.25 f 3.31"
8.27 f 5.73"
11.76 f 6.34b
14.51 f 5.03b
14.79 f 4.42b
7.28 f 3.42"
15.6
Ventricular wallz
thickness (mm)
VS/LV2
RV
LV
4.1 f 1.7
4.0 f 1.7
3.9 f 1.4
4.7 f 2.2
3.8 f 1.2
4.1 f 1.3
3.0 f 1.4
4.0
vs
10.4 f 4.4
10.6 f 4.8
10.2 f 4.3
11.7 f 4.8
7.6 f 3.5
7.4 f 2.6
7.6 f 3.2
5.5
11.4 f 4.7
11.4 f 4.9
11.0 f 4.4
12.4 f 5.1
8.7 f 3.5
7.8 -+ 2.2
8.0 f 3.4
5.8
1.09 f 0.06"
1.09 f 0.08"
1.09 f 0.06"
1.07 f 0.13"
1.16 f O.lOb
1.07 f 0.11"
1.05 f 0.06"
1.1
Comparison between normal and other heart anomalies: entries in the same column with
different superscripts (" and b, are different at P < .01.
Ratio of heart weight (gm) to body weight (kg).
Thickness of right ventricular wall (RV), left ventricular wall (LV), ventricular septum
(VS), and ratio of the thickness of VS to LV.
From one day to four years of age.
-+ = Standard error; TD = dysplasia of the tricuspid valve; ASD = atrial septal defect; SAS
= subaortic stenosis; VSD = ventricular septal defect; A-V canal = persistent common
atrioventricular canal; MMB = malformation of moderator band; PTA = persistent truncus
arteriosus.
persistent common atrioventricular canal in seven pigs, dysplasia of the tricuspid
valve in four pigs, and subaortic stenosis in two pigs.
Subaortic stenosis was diagnosed in 22 pigs, and 14 (70%) had single anomalies.
The 14 affected pigs ranged from 30 days to 7.5 months of age. Nine of the 14
affected pigs were male.
There was significant increase (P < .01) in relative heart weight in pigs with
subaortic stenosis (1 1.76 & 6.34 gm/kg), as compared with pigs with normal hearts
(6.28 f 3.18 gm/kg) (table 111). The mean thickness of left ventricular wall (11.7 f
4.8 mm) and ventricular septum (12.4 & 5.1 mm) in the affected pigs were increased,
but were not significantly different from normal pigs (table 111). Ratio of ventricular
septum to left ventricular wall was 1.07 f 0.13.
The defect was characterized by the presence of a fibrous collar encircling the left
ventricular outflow tract 0.5 to 1.5 cm below the aortic valve, with great variation in
severity (fig. 4). In the eight pigs with severe lesions, the thickened endocardia1 collar
or membrane extended from the base of the anterior leaflet of the mitral valve to the
aortic valve. Constriction of the annulus and dilatation of the supra-valvular area
were observed. In the six pigs with mild to moderate lesions, a narrow ring of white,
fibrous endocardium extended partially around the left ventricular outflow tract. The
ring primarily originated at the base of the anterior leaflet of the mitral valve and
extended transversely across the interventricular septum for a variable distance.
Of the 14 pigs with subaortic stenosis, seven pigs had left ventricular hypertrophy
and four pigs had left ventricular dilatation, ten of the affected pigs had left atrial
Congenital Heart Diseases in Swine
68 1
6
8
Fig. 5: Subaortic stenosis from same pig as fig. 4. Discrete membrane of fibrous tissue (me)
on superficial endocardium in outflow tract. HE.
Fig. 6 Photomicrograph of abnormal intramural coronary artery from pig with subaortic
stenosis. Marked thickening of vessel wall with narrowing of lumen. HE.
Fig. 7: Left side of heart from 25-day-old pig with ventricular septal defect.
Fig. 8: Right side of heart from 56-day-old pig with persistent common atrioventricular
canal of the transitional type with large defect (D) and cleft (arrow) at junction of septal and
anterior leaflets of tricuspid valve.
hypertrophy, and three had both left and right ventricular hypertrophy. The heart
wall of the remaining three pigs was of normal thickness.
Microscopically, a well-developed subvalvular ring or membrane consisting of
fibrous connective tissue and elongated fibroblastic cells, was present on the left
ventricular outflow tract (fig. 5).
Severe changes of the intramural coronary arteries (fig. 6 ) occurred in nine of the
pigs with subaortic stenosis. These changes consisted of marked increase in vessel size with a luminal narrowing, intimal fibromuscular proliferation, and disorganiza-
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Fig. 9 Abnormal heart (right) with malformed (thin. stringlike) moderator band (arrow)
attached to deformed trabecule. Normal heart (left) for comparison.
tion of the media. Occasionally, foci of myocardial necrosis with or without fibrosis
were found, involving the left ventricular wall and ventricular septum.
The anomaly was accompanied by vegetative endocarditis in four pigs, fibrous
thickening of both mitral and tricuspid valves in two pigs, atrial septal defect in two
pigs, ventricular septal defect in two pigs, and persistent common atrioventricular
canal in three pigs.
Ventricular septal defect was diagnosed in nine pigs from seven to 125 days of age.
Six of the nine affected pigs were male.
The relative heart weight in pigs with ventricular septal defect was 14.5 f 5.03
gm/kg (table 111), which is greater (P < .01) than in pigs with a normal heart (6.28
f 3.18 gm/kg).
All these defects, varying from 3 to 10 mm, occurred in the membranous portion
of the septum (fig. 7). Of the nine pigs with ventricular septal defect, two pigs had
left ventricular hypertrophy, and three pigs had left ventricular dilatation. The
remaining four pigs were normal on gross examination. Hypertrophy of the right
ventricle was seen in five pigs.
The abnormality was associated with atrial septal defect in seven pigs, with
dysplasia of the tricuspid valve in five pigs, with subaortic stenosis in two pigs, and
with vegetative endocarditis in two pigs. The mitral valves were normal on gross
examination.
Persistent common atrioventricular canal was diagnosed in eight pigs from 27 to
68 days of age. Two of the eight affected pigs were male. The relative heart weight
was 14.79 f 4.42 gm/kg (table 111), which was greater (P < .Ol) than in pigs with
normal heart (6.28 f 3.18 gm/kg).
The defects, varying from 6 mm to 20 mm, occurred in the lowermost portion of
the atrial septum and the uppermost portion of the ventricular septum at the level of
the coronary sinus. They were associated with malformation of the atrioventricular
valves. This defect caused interatrial and interventricular communication among the
four chambers of the heart (fig. 8).
Congenital Heart Diseases in Swine
683
Fig. 1 0 Right ventricle and great vessel from six-day-old pig with persistent truncus
arteriousus (Tr).
Of the eight anomalies, one was complete and seven were transitional. In the
complete lesion, both the anterior mitral and septal tricuspid leaflets were cleft. The
mitral valve was continuous with the tricuspid valve and was not attached to the
upper edge of the ventricular septum, whereas in the transitional lesions, both the
septal tricuspid and anterior mitral valves were cleft. The cleft valves were thickened
and attached abnormally to the ventricular septum.
Persistent atrioventricular canal was accompanied by: subaortic stenosis in the two
pigs, pulmonary stenosis in one pig, vegetative endocarditis in one pig, and persistent
left anterior vena cava in one pig. In the case of pulmonary stenosis, the pulmonary
valve was dysplastic and markedly stenotic. The lesions resulted in marked supravalvular dilatation of the pulmonary artery.
Malformation of the moderator band in the right ventricle was diagnosed in seven
pigs. All were males from seven to 163 days of age. Five pigs were under two months
of age, including two pigs which were seven days of age. The relative heart weight
(7.28 f 3.42 gm/kg) in the seven affected pigs was greater, but not significantly
different from that in the pigs with a normal heart (table 111).
All 1906 pigs examined in this study had a muscular moderator band in the right
ventricle of the heart (fig. 1, 9). It extended between the anterior papillary muscle of
the ventricular septum and the lateral papillary muscle.
The malformation of the moderator band of the seven affected pigs were all
muscular, but the appearance varied. Three of the seven affected pigs had two stout,
parallel bands, which extended from the lateral papillary muscle into the anterior
papillary muscle of the ventricular septum. Fusing of the two abnormal bands at the
mid portion was observed. Among the seven affected pigs, two had two to three
branches on the band at the lateral papillary muscle end, one had a big cord-like
684
Hsu and Du
band, and the remaining one had a normal-sized band, but it started at the lateral
papillary muscle and extended to the ventricular trabeculae.
Persistent truncus arteriosus was found in a six-day-old, female, Large White
crossbred Landrace pig. The anomaly consisted of a gross ventricular septal defect,
atrial septal defect, and biventricular origin of a single great vessel (31-mm circumference) (fig. 10). This anomaly was accompanied by persistent cranial vena cava.
Discussion
The data accumulated here show the incidence of congenital heart diseases in the
necropsied pigs only, and the prevalence rate of the anomalies in the general
population of swine remains unknown, since no live pigs were examined.
The incidence of congenital heart disease found in this study (4.35%) was higher
than one report (0.49%) [23], but lower than the results (14.6%) reported in a herd
surveyed for a short period of time [20], whereas the prevalence rate of the defect in
man [19], dogs [16], and cats [12], was 1%, 0.68%, and 0.17%, respectively.
In this study, the congenital heart disease was found to be higher in the group of
pigs 29 to 110 days of age than in pigs in other age groups. This might indicate that
pigs with congenital heart disease commonly would die within this age period. Young
children [8], dogs [4], and cats [12] less than one year of age with cardiac anomalies
develop signs of acute heart failure.
The prevalence of congenital heart disease is higher in purebred than in mixed
dogs and is higher in certain breeds than in the general population [16]. The latter
findings were not found in our study of swine. This may have been because too few
purebred pigs were observed to permit any conclusions.
From this study, it is not possible to determine whether the prenatal status of the
sows contributed to the cardiac anomalies. It is thought that congenital disease in
dogs and man results from single recessive genes or polygenic sets that have lesionspecific effects on cardiac development [5, 16, 171.
Many types of congenital heart disease, such as dysplasia of the tricuspid valve,
subaortic stenosis, atrial septal defect, ventricular septal defect, persistent common
atrioventricular canal, persistent truncus arteriosus, persistent cranial vena cava, and
pulmonary stenosis, which occur spontaneously in man [5, 191, dogs [17], and cats
[12] were observed in pigs in this study, but some types, such as patent ductus
arteriosus, tetralogy of Fallot, Ebsteins’s malformation, and mitral insufficiency,
which are common in man [5, 191 and small animals [12, 161, were not observed in
pigs.
Dysplasia of the tricuspid valve is the most important heart disease in swine and
it occurred in the swine in this study with predominance at 29 to 56 days of age,
while in dogs and cats, the predominance was at 5.4 and 6.7 months, respectively
~141.
The changes of tricuspid valvular dysplasia observed in the 42 pigs in this study
were very similar to those in man [ 11 and in small animals [ 141. The abnormalities
differed from Ebstein’s malformation by the absence of downward displacement of
Congenital Heart Diseases in Swine
685
the basal attachment of the leaflet [5]. This may result from a developmental arrest
at some stage or incomplete development of the cardiac valve in fetal life [7].
The morphological alterations of subaortic stenosis in the pigs in this study were
similar to those previously reported in man [5], dogs [15, 16, 181, pigs [6, 201, and
cows [lo]. The etiology of subaortic stenosis in pigs is unknown. In man and dog, the
anomaly usually is considered to be a congenital defect. Previous investigators [ 15,
181 think that discrete subaortic stenosis is inherited as a specific gene defect in
Newfoundland dogs.
Subaortic stenosis in man [5] and Newfoundland dogs [ 15, 181 often is complicated
by infectious endocarditis. This also happens in pigs. Abnormalities of the intramural
coronary arteries similar to those occurring in the ventricular septum of the pigs with
subaortic stenosis also were observed in pigs with hypertrophic cardiomyopathy
(Hsu, F.S., unpublished data).
The morphological changes of ventricular septal defects in the membranous septum
of the pigs in this study were similar to those reported in man [5], small animals [4,
12, 161, and cattle [2] with ventricular septal defect, whereas in sheep the defect was
in the muscular septum [3].
The features of persistent common atrioventricular canal found in this study also
were similar to those reported in man [5, 191 and small animals [12, 131. The etiology
of persistent common atrioventricular canal is thought to be an embryologic malformation of the endocardial cushions. The hearts of 59 patients with persistent common
atrioventricular canal malformations were examined and it was reported that the
septum of atrioventricular malformation may arise as a result of reduced compression
of the developing atria by surrounding structure during the embryonic stage [9].
It was reported that the complete and partial varieties of persistent common
atrioventricular canal appear to represent different degrees of malformation in
relation to the atrioventricular endocardial cushions, while transitional varieties
present an intermediate degree of malformation [22].
Others indicated that a normal moderator band is present in the right ventricle in
man, pigs, cattle, and dogs [21]. The development in pigs is exceedingly variable; it
may be a long thread-like cord consisting almost entirely of Purkinje fibers, or it may
be short and thick with a predominant amount of cardiac myofibers.
The abnormalities of porcine persistent truncus arteriosus found in this study also
were similar to those observed in man [5] and small animals [ 121.
Enlargement of heart, passive congestion of visceral organs, ascites and hydropericardium consistently were observed in the cases of subaortic stenosis, atrial septal
defect, ventricular septal defect and persistent common atrioventricular canal.
The study also indicates that vegetative endocarditis commonly accompanied
subaortic stenosis, ventricular septal defect, and persistent common atrioventricular
canal. Seventy percent of the cases are related to streptococci.
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Request reprints from Dr. F.S. Hsu, Animal Industry Research Institute, TSC, Chunan,
Miaoli, Taiwan 350, (Republic of China).