Comp. Immun. Microbiol. infect. Dis. Vol. 15, No. 3, pp. 203-211, 1992 Printed in Great Britain
0147-9571/92 $5.00+0.00 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, DISEASE AND PATHOLOGY
CLINICAL
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
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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 Country Austria Belgium Denmark France Fed. Rep. G e r m a n y Greece Irish Republic Italy Luxembourg Netherlands Portugal Spain Switzerland United K i n g d o m Yugoslavia - - N o data available.
1980 . 7 0 19 18 -0 0 0 0 267 40 0 0 15
1981 . 37 0 6 4 20 0 5 8 11 506 84 0 0 0
N u m b e r o f confirmed outbreaks per year 1982 1983 1984 1985 1986 . 102 0 8 19 4 0 40 1 70 176 24 0 0 0
.
.
26 0 13 535 2 0 48 1 150 82 7 0 0 0
9 0 19 1041 3 0 12 0 169 28 I 0 0 22
1987
1988
1989
83 0 5 41 0 0 -1 1 0 0 0 1 18
0 2 0 16 3 0 0 12 0 0 0 0 0 0 13
15 8 0 0 64 0 0 1I 0 0 0 0 0 0 --
. 67 0 2 351 1 0 27 0 36 3 1 0 0 141
80 0 20 46 0 0 29 0 0 0 0 0 3 39
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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
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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.
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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 investigations 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
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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
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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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49. Liess B. Persistent infections of hog cholera: a review. Prevent. vet. Med. 2, 109-113 (1984). 50. Frey H. R., Liess B., Richter-Reichhelm H. B., von Benten K. and Trautwein G. Experimental transplacental transmission of hog cholera virus in pigs I. virological and serological studies. Zbl. vet. Med. B27, 154-164 (1980). 51. Meyer H., Liess B., Herrmanns W. und Trautwein G. Experimentelle, diaplazentare Infektion von Schweinefeten mit dem Virus der Europ~iischen Schweinepest (ESP). Virologische und serologische Untersuchungen in der postnatalen Phase. Fortsch. Veteriniirm. 30, 140-144 (1980). 52. Meyer H., Liess B., Frey H. R., Herrmanns W. and Trautwein G. Experimental transplacental transmission of hog cholera virus in pigs. IV. Virological and serological studies in newborn piglets. Zbl. vet. Med. 2,8B, 659-668 (1981). 53. Van Oirschot J. T. and Terpstra C. A congenital persistent swine fever infection. I. Clinical and virological observation. Vet. Microbiol. 2, 121-132 (1977). 54. Van Oirschot J. T. Congenital swine fever infections. Preliminary results. In Hog Cholera/Classical Swine Fever and African Swine Fever (Edited by Liess B.), pp. 184-199. Commission of the European Communities, Brussels, Publication EUR 5904 (1977). 55. Liess B. Bedeutung der Immuntoleranz fiir die Pathogenese der bovinen Virusdiarrhoe (BVD). Berl. Miinch. tieriirztl. Wschr. 8, 420-423 (1985). 56. Liess B. Viruspersistenz---ein Schliisselph~nomen der BVD-Virusinfektion. Dtsch. tieriirztl. Wschr. 95, 264-266 (1987). 57. Cheville N. F. and Mengeling W. I. The pathogenesis of chronic hog cholera (swine fever). Histologic, immunofluorescent, and electron microscopic studies. Lab. Invest. 20, 261-274 (1969). 58. Trautwein G. Pathology and pathogenesis of the disease. In Classical Swine Fever and Related Infections (Edited by Liess B.), pp. 27-54. Nijhoff, Dordrecht (1988). 59. Weide K. D., Waxier G. L., Whitehair C. K. and Morrill C. C. Hog cholera in gnotobiotic pigs clinical signs and gross pathological findings in germfree and monocontaminated pigs. J.A.V.M.A. 140, 1056-1061 (1962). 60. Luedke A. J. and Dunne H. W. Focal necrosis in the mucosa of the gall bladder in pigs with hog cholera. Am. J. vet. Res. 22, 391 395 (1961).
0147-9571/92 $5.00+0.00 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, DISEASE AND PATHOLOGY
CLINICAL
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
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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 Country Austria Belgium Denmark France Fed. Rep. G e r m a n y Greece Irish Republic Italy Luxembourg Netherlands Portugal Spain Switzerland United K i n g d o m Yugoslavia - - N o data available.
1980 . 7 0 19 18 -0 0 0 0 267 40 0 0 15
1981 . 37 0 6 4 20 0 5 8 11 506 84 0 0 0
N u m b e r o f confirmed outbreaks per year 1982 1983 1984 1985 1986 . 102 0 8 19 4 0 40 1 70 176 24 0 0 0
.
.
26 0 13 535 2 0 48 1 150 82 7 0 0 0
9 0 19 1041 3 0 12 0 169 28 I 0 0 22
1987
1988
1989
83 0 5 41 0 0 -1 1 0 0 0 1 18
0 2 0 16 3 0 0 12 0 0 0 0 0 0 13
15 8 0 0 64 0 0 1I 0 0 0 0 0 0 --
. 67 0 2 351 1 0 27 0 36 3 1 0 0 141
80 0 20 46 0 0 29 0 0 0 0 0 3 39
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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
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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.
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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 investigations 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
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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
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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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