Comp. Immun. Microbiol. infect. Dis. Vol. 15, No. 3, pp. 203-211, 1992 0147-9571/92 $5.00+0.

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Printed in Great Britain Pergamon Press Ltd

A REVIEW O N C L A S S I C A L S W I N E FEVER
INFECTIONS IN PIGS: EPIZOOTIOLOGY, CLINICAL
DISEASE AND PATHOLOGY

J. DAHLE a n d B. LIESS
Institute of Virology, Hannover Veterinary School, Bfinteweg 17, D-3000 Hannover l,
Fed. Rep. Germany

Abstract--A review is given on classical swine fever (CSF) including epizootiology, clinical disease
and pathology. Under the item o f epizootiology the history of CSF is briefly summarized. Ways
of transmission are described with special reference to CSF in wild boars. The chapter about clinical
disease includes the description of different courses of CSF such as peracute, acute, subacute form
and chronic disease with reference to the course o f transplacental infection and fate of the progeny
associated with the "carrier sow syndrome". The most typical lesions in CSF are summarized in
the chapter of pathology.

Key words: Classical swine fever, hog cholera, epizootiology, clinical disease, pathology.

UNE REVUE SUR LES INFECTIONS DE FII~VRE PORCINE

CLASSIQUE CHEZ LE PORC: t~PIZOOTIOLOGIE, MALADIE
CLINIQUE ET PATHOLOGIE

R r s u m r - - L ' o n donne une revue sur la firvre porcine classique (CSF: classical swine fever)
comprenant l'rpizootiologie, la maladie clinique et la pathologie. Sous l'article 6pizootiologie,
l'histoire de la CSF est brirvement rrsumre. Les moyens de transmission sont drcrits en particulier
en ce qui concerne la CSF chez le sanglier sauvage. Le chapitre traitant de la maladie clinique
comprend la description des diffrrents cours de la CSF, tels que les formes suraigu~, aigu~ et
subaigu~ et la maladie chronique, avec rrfrrence au cours de I'infection transplancentaire et au sort
de la progrniture associre au "syndrome de la truie porteuse'. Les 16sions les plus typiques de la
CSF sont rrsumres dan le chapitre de la pathologie.

Mots-clefs: Peste poricine classique, cholrra du porc, 6pizootiologie, maladie clinique, pathologie.

INTRODUCTION

Classical swine fever (CSF) is an infectious viral disease that may occur in domestic pigs
and wild boar under natural conditions. The disease has played an important economic
role mainly in countries with a dense pig population. The international terminology has
used different synonyms such as hog cholera (HC) at the first report in the U.S.A., swine
fever (SF) or "European" swine fever in Europe, and classical swine fever (CSF) in contrast
to African swine fever (ASF). The actual designation is "classical swine fever (CSF)" for
the disease (FAO-WHO-OIE, Animal Health Yearbook, 1978) and "hog cholera virus
(HCV)"* for the infectious agent [1].

* W H O - F A O programme on comparative virology, report "small enveloped RNA viruses working team",
16-18 November, Budapest 1976.

203
204 J. DAHLE a n d B. LIESS

EPIZOOTIOLOGY
The early appearance of hog cholera has been placed in Ohio in the 1833. Hanson [2]
reviewed the available information on the real origin of the disease. The first document
was published in 1888 as part of the Fourth and Fifth Annual Report of the Bureau of
Animal Industry. It was a compilation from reports of correspondents of the U.S.
Department of Agriculture describing observations on the new disease during the period
from 1818 to 1888. For the origin one author assumed "that the contagion was imported
from Europe with some of the animals that were brought from there to improve our breeds
of swine". This statement was disagreed by European authorities and never proved to be
right or wrong. Historically the real origin of hog cholera/classical swine fever remains
unclear. Reports on the occurrence of CSF in European countries commenced at the end
of the last century. At that time Great Britain experienced a large number of outbreaks
and CSF was made a notifiable disease since 1879 [3]. From Fed. Rep. Germany statistical
data are available since 1899 [4] and up to today like in other countries the disease has
never been totally eradicated. In countries with intensive pig industries the classical swine
fever situation has shown that years with numerous outbreaks may be followed by
CSF-free periods or decreasing numbers of outbreaks. During more than 90 yr the course
of CSF in Fed. Rep. Germany has shown extreme variations with peaks of outbreaks in
1906 (21,918), 1913 (13,574), 1922 (5673), 1927 (3975), 1930 (4600), 1939 (5688), 1951
(2912), 1962 (2366), 1966 (1908), 1973 (3936), 1984 (1041) [4, 5].
The worldwide distribution of CSF included North and South America, Europe, Asia,
Africa and Australia. Eradication has been successful in Australia since 1963, Canada
in 1964 and U.S.A. in 1977. In Europe CSF still remains a problem in some countries
(Table 1) but at the end of 1989, France, Greece, Luxembourg, Netherlands, Portugal,
Spain, and the U.K. reported freedom from CSF. No cases of CSF were reported in
Denmark (since 1933), the Republic of Ireland (since 1956), and Switzerland (since 1974).
Under natural conditions domestic pigs and wild boar are known to be susceptible to
CSF infections [6]. In general, piglets used to be more severely affected than adult animals.
Animal experiments proved that the host range of HCV is extended to ruminants.
Inoculation into peccaries, cattle, goats, sheep and deer led to subclinical infections [7, 8].

Table 1. Classical swine fever outbreaks in European countries within a period of 10 yr from 1980 to 1989. D a t a obtained by
courtesy of E E C National Swine Fever Laboratories and by Classical Swine Fever Reference Laboratories of EEC non-member
states
N u m b e r o f confirmed outbreaks per year
Country 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989
Austria . . . . . . 0 15
Belgium 7 37 102 26 9 67 80 83 2 8
Denmark 0 0 0 0 0 0 0 0 0 0
France 19 6 8 13 19 2 20 5 16 0
Fed. Rep. G e r m a n y 18 4 19 535 1041 351 46 41 3 64
Greece -- 20 4 2 3 1 0 0 0 0
Irish Republic 0 0 0 0 0 0 0 0 0 0
Italy 0 5 40 48 12 27 29 -- 12 1I
Luxembourg 0 8 1 1 0 0 0 1 0 0
Netherlands 0 11 70 150 169 36 0 1 0 0
Portugal 267 506 176 82 28 3 0 0 0 0
Spain 40 84 24 7 I 1 0 0 0 0
Switzerland 0 0 0 0 0 0 0 0 0 0
United K i n g d o m 0 0 0 0 0 0 3 1 0 0
Yugoslavia 15 0 0 0 22 141 39 18 13 --
- - N o data available.
 Review on classical swine fever infections in pigs 205

Serial passages of HCV between pigs and laboratory rabbits [9, 10] resulted in adaption
of several strains to the rabbit. One lapinized strain (C-strain) was produced in China by
more than 400 serial passages and was established as HC-vaccine strain [11, 12].
The most important route of natural transmission seems to be the oral or nasal as shown
under experimental conditions [13, 14]. Pigs infected with a high virulent strain excrete the
virus from mucous membranes, e.g. oronasal cavities, urogenital tract, alimentary tract,
conjunctiva fluids [14, 15].
The spreading of the disease is supported by movement of virus excreting pigs within
a dense population. Purchase of weaners from different breeding farms to fattening units
or to markets [16] always carry a high risk of introducing the virus into susceptible pigs.
Especially low virulent strains may be propagated unnoticed on "carrier sows" and be
spread by trade almost unnoticed [17]. Short periods of virus excretion and following
antibody response have been observed in postnatal infections with low virulent strains.
Insects as possible vectors for CSF have been reported. Experiments carried out by
Dorset et al. [18] showed that house flies (Musca domestica) and stable flies (Stomoxys
calcitrans) could transmit HCV by contact with the eyes or skin injuries. Observations
indicating that HCV was transmitted from a stable containing infected pigs to pigs in a
neighbouring stable were reported by Reuss [19].
Another way of HCV transmission from lungworms to earthworms and back to swine
has been shown under experimental conditions [20, 21] but could not be verified by
Solorzano and Thigpen [22]. CSF could be transmitted under experimental conditions by
Trichinella spiralis larvae isolated from diaphragma tissue of CSF-affected pigs [23, 24].
In areas of high density of pig population transmission by man may be an important
factor [25] by spreading the virus with contaminated instruments and drugs used by
farmers, castrators, inseminators, vaccination teams and veterinarians. In the epizootic
from 1971 to 1974 in Hessen, Fed. Rep. Germany, the veterinary authorities concluded
that a iatrogenic transmission was responsible in a total of 19 districts and 38 holdings
[26].
Pork and pig products [27, 28] are a reservoir for HCV and play an important role in
transmission of the disease. The survival of HCV may be prolonged in protein-rich
environment especially in cooled or frozen products [29, 30]. The habit of feeding garbage
from restaurants or barracks [4, 31, 26] to pigs often has been reported to be a source of
CSF outbreaks in fattening farms but also in small holdings [32].
The role of wild living pigs as a virus reservoir has been discussed by various authors.
In serum samples taken from feral pigs in Australia antibodies against HCV were detected
by gel diffusion precipitin test [33]. The epizootiology of CSF in European wild boar still
needs intensive investigation. Contacts to wild boars may occur directly when domestic
pigs are kept outside [34]. In the CSF-epizootic in Hessen from 1971 to 1974 a total of
10.6% of outbreaks were traced back directly or indirectly to wild boar [26]. Closer
epizootiological investigations revealed, however, that garbage from American barracks as
well as porcine slaughter offal had been used as baits during the hunting season. It is
assumed that the source of infection of wild boar population originated in those offals but
that on the other hand in the following domestic pigs were infected by feeding the offals
of wild boar carcasses left by the hunters. In one case a captured young boar was kept
on a pig farm and was held responsible for infecting the holding [35]. The present CSF
epizootic in wild boars that was confirmed in the autumn of 1989 in Hessen delivered
another rather obscure information saying that a sick young boar was captured by a pig
206 J. DAHLE and B. LtESS

farmer and nursed in his holding (communication of the Federal Ministry of Agriculture,
Bonn, Fed. Rep. Germany). After recovery the animal was set out in the woods again and
short time later CSF was confirmed in the holding. A possible link of CSF outbreaks in
wild boar in the Odenwald (Fed. Rep. Germany) in 1951 may be suspected in primary
outbreaks in domestic pigs that occurred before in that region. Two owners of
CSF-affected farms admitted that they had buried or thrown dead piglets in the nearby
wood [34].
Up to today the epizootiological role of wild boar as a reservoir for HCV is questionable.
Results of a serological screening carried out with blood samples of killed wild boar in
Lower Saxony during the hunting season of autumn 1990 to spring 1991 lead to the
assumption that under natural conditions the wild boar population is free of antibodies
against HCV (Patzelt et al., in preparation).

CLINICAL DISEASE
The clinical picture of CSF is not always characterized by a febrile disease with typical
clinical signs and high morbidity and mortality. In 1961 it has been warned by Reppin [36]
that an atypical form may occur unnoticed in affected holdings and clinical and
pathological diagnosis are not sufficient to confirm the disease.
Overall four forms of classical swine fever have been described:
the peracute form yielding a high morbidity and death within 5 days post
infection [37],
the acute form terminating in death between 10 and 20 days post infection [37],
the subacute form terminating in death between 20 and 29 days post infection [37],
and
the chronic disease, duration of 30 or more days [38].
Different factors have been discussed to influence the course of a HCV infection. It is
known that strains and field isolates from different outbreaks use to show variations
in virulence and pathogenicity. Van Oirschot [39] differentiated in (i) high-virulent,
(ii) moderate-virulent and (iii) avirulent HCV strains. Due to his definition, high-virulent
strains kill nearly all pigs, irrespective of age; moderate-virulent strains generally lead to
subacute illness in postnatally infected piglets but may cause abnormalities in porcine
foetuses; and avirulent strains are attenuated and virtually apathogenic for foetuses.
This classification contradicts the findings of other authors. Mengeling and Cheville[ 38]
and Liess et al. [40] observed that the degree of pathogenicity varied from one pig to
another. In animal experiments low virulent HCV strains induced both subacute disease
with classical lesions as well as a transient form with recovery and immunity. Experimental
data have shown that the age of the animals may influence the course of an infection.
Inoculation in young pigs with low virulent HCV strains led to high mortality and heavy
losses in young pigs and recovery in older pigs [41]. Another factor influencing the course
of disease is the virus dose applied to an animal. A hog cholera virus titration in weaner
pigs using the high virulent strain "Alfort" showed that the minimal infective dose
resulting in fatal disease was less than 10 TCIDs0 per pig [42]. At the highest log~0 dilution
step of virus at which fatal disease occurred one out of four animals died whereas the
surviving pigs developed neutralizing antibodies.
 Review on classical swine fever infections in pigs 207

Peracute, acute and subacute f o r m

The peracute form is characterized by a rapid course without typical clinical signs
suspect for CSF followed by sudden death [43]. The activity of affected animals decreases,
anorexia may be observed in the early stage of disease. Body temperature usually rises and
surmounts 40°C within 2-6 days post exposure to the virus [37] with a usual peak between
the fourth and eighth day of illness. In the following exudative conjunctivitis may occur,
affected pigs use to huddle and pile in a corner of the stable. After 4-8 days vomiting may
be followed by constipation with hard faecal pellets intermittent with watery, yellowish
diarrhea. In acute cases incoordination of movements leads to a weaving and staggering
gait due to the weakness of the animal. In rare cases, convulsions may be associated with
CSF [37, 43]. The clinical signs start with a stiffening of the body, followed by prostration
and violent running movements. Sporadic actions or continuous convulsions may occur.
In typical acute courses prominent clinical signs appear in the skin of white pigs.
Preceding hyperemia of the skin may be followed by petechial or extensive haemorrhages
as well as cyanosis of the ears. In subacute or chronic cases a blotching of the ears has
been described [37].

Chronic disease
Chronic disease and sublethal course in CSF have been first reported by Nusshag [44]
and Michalka [45]. Due to the definition by Mengeling and Cheville [38] chronic CSF
performs a lethal clinical form terminating in death after 30 or more days.
Chronic or persistent CSF, respectively, may occur both after prenatal or postnatal
infection of pigs.
Postnatal infections have been seldom reported to cause persistent and chronic infections
[40, 46] but may be important. Intensive field and experimental investigations have been
initiated by the "pregnant carrier sow syndrome" [17] and focussed the main interest on
transplacental and prenatal infection. Ellis et al. [47] reported on a French survey
concentrated mainly on Brittany with 46% of some hundred sows that had shown
reproductive failure were found to be serologically positive for CSF. Serological investi-
gations of sera sampled in 346 breeding farms out of three villages with no clinical signs
reported led to the detection of 5.4% seropositive pigs [48]. The infecting strains are mostly
classified into the group of the so-called "low virulent" strains. Strains that cause chronic
infection of the progeny must lead to a subclinical infection in the sow and be transmissible
to the foetuses via placenta [49]. Under experimental conditions the " G l e n t o r f " strain
[40, 50-52] and the "Bergen" strain [53] both fulfilled this requirement. The American
HCV strain "331" [38] that induced chronic disease in pigs between 2 and 8 months of
age has not been proven to be transmissible transplacentally. As it has been pointed out
before, postnatal infections play a minor role in chronic infection. In most cases a
congenital infection in utero by transplacental transmission is responsible for a lifelong
virus persistence in the litter. Experiments with the Glentorf strain showed that the result
of a transplacental infection depends on the day of gestation the sows are infected [51].
Inoculation at early stage of gestation up to 70 days lead to stillborn or aborted foetuses
with typical lesions and/or demonstration of HC viral antigen. Persistent infections of the
litters were exclusively observed when sows had been inoculated between 70 and 90 days
of gestation. After transplacental transmission in sows a total of 82 piglets were farrowed
including 30 (36%) that were born viraemic. Within 2 weeks post partum 21 (25%) died
208 J. DAHLEand B. LIESS

whereas 9 piglets (11%) survived for 3-8 weeks, respectively. The viraemic piglets excreted
virus up to 2 weeks but as they did not show any clinical signs it was not possible to identify
them amongst their non-viraemic littermates. A chronic form of disease developed later
and the animals died within 3-8 weeks of age. Piglets that were not infected at birth
remained healthy and after the decline of maternal antibody developed neutralizing
antibodies against HCV due to their contact with virus excreting littermates. Investigations
with the Bergen strain led to similar results [54] with persistently infected piglets living up
to 153 days post partum. It should be mentioned hereby that virus persistence induced by
transplacental infection is a common problem in pestiviruses and has been reviewed for
BVD virus infections in cattle [55, 56]. Infection of bovine foetuses after 90 days of
gestation leads to a lifelong protection by development of neutralizing antibodies. A
transplacental virus transmission up to the end of third month of pregnancy, however, does
not induce neutralizing antibodies and may infect the immune tolerant foetus. The
postnatal fate of those calves may result in normal development of the animal giving birth
to (1) immune tolerant calves normally or weakly developed, (2) perinatal or postnatal
illness with death up to 2 months, (3) chronic infection apparent by growth retardation
and runting and (4) acute disease showing up in bovine viral diarrhoea or mucosal disease,
respectively, usually between 8 months and 2 yr post partum or more after preceding
permanent viraemia.

PATHOLOGY
Under natural conditions HCV normally enters the host organism by the oronasal route.
The tonsils are considered as the primary location for virus multiplication being followed
by the regional lymphnodes and after distribution by viraemia throughout the organism
the virus may be detected in different organs. In general, main target cells for HCV
multiplication are endothelial cells, lymphoreticular cells and epithelial cells [57]. Thus
in the classical course of CSF the affinity of the virus for endothelial cells causes
haemorrhagic diathesis with petechial haemorrhages in most organ systems and serous
membranes [58]. Inoculation in gnotobiotic pigs [59] was carried out in order to exclude
secondary bacterial infection. Necropsy revealed haemorrhages in the lymph nodes,
kidneys, lungs, meninges, diaphragm, stomach, heart as well as petechial haemorrhages of
the bladder mucosa as well on mucosa and serosa of the small intestine and the colon.
Gross lesions have been reviewed by Dunne [37]. In peracute cases it may be difficult to
discern any evidence for haemorrhages in an infected animal.
From outer adspection of the animal in an acute case of disease a typical sign is erythema
of the skin that can increase, mainly in ears or tail, to a cyanotic colour. Petechial or
ecchymotic haemorrhages of the skin may occur. In the early stage of the disease
pathological signs may be noticed in the lymphnodes beginning with enlargement and
edema. In the following, haemorrhages may appear in different types varying from
moderately red to almost black in colour. Pathological signs in the tonsils may appear as
a mild inflammation that develops later to a necrotic tonsillitis or, due to secondary
bacterial infection, to a suppurative tonsillitis. Petechial haemorrhages in the epiglottis and
larynx are typical signs. In the urinary tract the kidneys show pathological changes on the
subcapsular surface in form of small petechial haemorrhages. In the urinary bladder
petechial haemorrhages have been described in the majority of cases but ecchymotic
haemorrhages or suffuse haemorrhages may occur occasionally. In the gastrointestinal
 Review on classical swine fever infections in pigs 209

tract stomach, small a n d large intestine m a y be affected. The f u n d u s region o f the stomach
m a y be haemorrhagic, in the m u c o s a mild or severe erosions m a y develop. I n the small
intestine pathological changes usually are limited to a mild to m o d e r a t e catarrhal enteritis
whereas in the large intestine the pathological signs use to be more p r o m i n e n t . B u t t o n
ulcers o f the colon are considered typical lesions for CSF. The early lesion begins as a small
necrotic area with a d h e r e n t faecal plaques. I n the following the ulcer shows concentric lines
a n d by secondary bacterial infection a n d the lesion becomes larger a n d encrusted with
m u c u s c o m b i n e d with cellular a n d faecal debris. In n a t u r a l infection the livers o f affected
pigs are generally dark, congested a n d swollen. Small areas of infarction due to t h r o m b o s i s
o f i n t e r l o b u l a r b l o o d vessels have rarely been observed. Luedke a n d D u n n e [60] described
small ulcer-like lesions o n the m u c o s a of the gall bladder.
A n o t h e r p a t h o g n o m o n i c lesion in C S F is infarction of the spleen.
Macroscopically variable sized dark blebs m a y be f o u n d on the periphery a n d the apex
of the spleen.
The c h r o n i c disease usually shows a n o t h e r pathological picture. A single o r g a n system
(lung, gastro-intestinal tract, central n e r v o u s system) m a y p r e d o m i n a n t l y be affected a n d
secondary bacterial infections m a y be involved [58]. B u t t o n ulcers as described above m a y
be present a n d followed by a diffuse diphteroid-necrotizing enteritis. In lymph nodes the
pathological signs m a y only consist in hyperplasia instead of typical h a e m o r r h a g e s as
described before in acute course o f disease.

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