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Principal
Features of the Epidemiology of Aujeszky’s
Disease – Suid herpesvirus 1 Infection – in Swine and Cattle.
Respiratory airborne and genital infections
have occurred worldwide in swine and cattle and there is strong evidence that
vaginal infection of cattle resulting in pruritus on the hindquarters had
regularly been sexually transmitted from sows by man.
Viggo Bitsch
© 2015 Viggo Bitsch
Abstract
Aujeszky's disease – infection with Suid
herpesvirus 1 (SuHV1) – is an infection of pigs, which under certain
conditions can be spread to several other animal species, usually with a fatal
outcome. It has been found worldwide but has now been eradicated in several countries. Denmark is the country,
where Aujeszky's disease has been studied most intensively, and the results
from investigations of cattle have been of greatest importance for understanding the epidemiology of the infection in swine. Denmark was the
first country to initiate eradication and the first to complete
eradication of the indigenous infection. In this review, important features are
recapitulated at the end of each section or subsection.
In cattle, the infection will most often give rise to an intense
pruritus of a skin area. In iatrogenic cases, the site of virus introduction will determine the site of pruritus but naturally, pruritus will appear (1) in the head region or on the chest,
which is associated with respiratory infection, or (2) on the hindquarters of
females, which indicates vaginal infection. In cases of respiratory infection, the virus can be found in the mucous membranes of the nasal or pharyngeal cavity of
animals with head pruritus, while in cases with chest pruritus virus can be
found in lung tissue. In cases with pruritus on the hindquarters, the virus will most often be found in the vagina.
Pruritus must be considered a phantom sensation due to stimulation or
damage of the central nervous system including sensory ganglia. Respiratory infection of cattle is a dead-end infection, as spread
among cattle has never been demonstrated. Relatively high virus titers found in mucous membranes in a few cases,
however, may be taken to indicate that transmission can not be totally
excluded.
The source of respiratory infection in cattle has always been pigs
infected by the respiratory route. Cattle at risk need not necessarily be those
placed near the infected pigs, as the virus in animal houses has been seen
transmitted by air currents determined by ventilators over distances of 10-20
meters, even from pigs in a neighboring room.
In swine, the infection was considered to be exclusively respiratory for decades, and naturally occurring genital infection was not demonstrated until 1981. In herds with outbreaks in cattle characterized by pruritus on the hindquarters (vaginal infection), respiratory infection of pigs was never observed, but a sow had characteristically been served by a foreign boar from 5-14 days earlier. In some such cases investigated, genital infection was confirmed in sows, which clearly linked cases in cattle with a posterior localization of pruritus to a concurrent genital infection of swine. A naturally occurring genital infection has been found also in wild pigs in the USA. Respiratory infection of pigs was demonstrated late in the history of the disease. The first outbreak in Denmark was in 1964, and in the preceding 33 years there had been only 3 outbreaks in cattle showing an anterior localization of pruritus indicative of respiratory infection, but close to 60 outbreaks, where the cattle showed a posterior localization of pruritus indicative of genital infection.
The development of the disease situation in pigs in Denmark has clearly illustrated that SuHV1 can change the degree of pathogenicity over time. The changes occurred in two steps. In the early 1960s, respiratory strains developed, which were spread rapidly between herds due to animal contacts, mainly by trade, and later in the 1970s strains developed, which had an even higher degree of pathogenicity for cattle and swine. These new strains were found syncytial in contrast to earlier isolates from traditional outbreaks. The new respiratory syncytial strains had not been introduced from abroad as restriction fragment pattern analyses of virus DNA documented that they possessed the Danish characteristics.
That syncytial virus strains were more virulent than non-syncytial
strains was later substantiated by results from examination of isolates from
England and Northern Ireland.
As
concluded from the studies of respiratory SuHV1 infection in cattle, the
decisive spread of the respiratory
infection among swine in a ventilated animal house will be by air currents over
many meters determined by the ventilation system and not by close
animal-to-animal contacts. This feature
also illustrates that during an acute outbreak in a swine herd, considerable
amounts of virus will be blown out into the surroundings by ventilators,
exposing neighboring herds to the risk of
infection. Early observations in Denmark led to the conclusion that airborne
spread between swine herds might occur over several kilometers and after
eradication of the indigenous infection, new infections were introduced from
abroad, which demonstrated that airborne spread of the virus between herds might take place over even 10 to 30 kilometers. Syncytial strains of SuHV1 have
shown to possess a pronounced tendency to airborne transmission among swine
herds, which implies that if a syncytial strain is first introduced into an area,
it is likely to become the prevailing type in that area within a few years.
The special manifestation of Aujeszky's disease in cattle showing pruritus on the hindquarters has regularly been associated with the use of a boar from a boar center for natural service of a sow shortly before the appearance of the clinical disease. In most cases examined, the virus was found in the vagina of the affected bovine animals, although in low titers, and in three outbreaks, the only cases investigated early enough to be likely successful, the virus was demonstrated in the vagina of a sow. It was found that animal sodomy seemed to play a role in the transmission of genital infection from swine to cattle, and this conclusion is further substantiated by supplementary information given in this review. From the fact that genital infection in cattle is closely correlated with contemporary genital infection in swine on the same premises and from the many reports over the years on infection in cattle showing pruritus on the hindquarters, it can additionally be concluded that the SuHV1 infection in a great part of the 20th century was maintained as a porcine genital infection in many countries.
1. Introduction
Suid herpesvirus 1 (SuHV1) infection or
Aujeszky’s disease was first identified as a new specific infectious disease in
Hungary by Aujeszky (1902). The
disease was found in a steer, a dog, and a cat from different premises, and all
showed pruritus in the nose and mouth area.
In the following years, the infection was reported in many countries, especially in cattle.
In Denmark, the infection was first seen in 1931 in cattle on two neighboring farms (Bang 1932). Five cows, one heifer, and two calves were affected. Five had pruritus on their heads, two on one side of the chest, while in a calf no itching was noticed. The source of infection for cattle was not identified. In 1932, Burggraaf and Lourens reported on a great number of affected cattle on 5 farms in Holland situated within a few kilometers from each other. They observed that the disease in cattle had been preceded by symptoms in swine. Pruritus was seen in the head or chest regions of the cattle. In 1935, Köves and Hirt reported natural, widespread infection in swine in Hungary, but already in 1913, the infection had been demonstrated in that country in a domestic sow suspected of rabies and in a wild pig forwarded for examination because of unspecific disease in the wild swine population in a certain wood district. Here, a similar disease problem had been observed the previous year. No wild pigs were then submitted for laboratory examination, but Aujeszky’s disease was diagnosed in a dog, a badger, and a fox from the district (Ratz 1914). Shope (1935a, b) found the infection to be widespread among swine in some areas in the USA and concluded that pigs were the source of infection for cattle. He had observed that the affected cattle had been kept in close contact with pigs and suggested that infection took occurred when nasal secretions from infected pigs were rubbed into the abraded skin of the cattle. This notion of cutaneous or percutaneous infection of cattle was concordant with the general experience from experimental infection of cattle, rabbits, etc. that pruritus would appear at the site, where the virus had been injected.
Denmark is
the country, where Aujeszky’s disease has been surveyed and studied most
intensively, not only right from its first appearance in 1931 until the
completed eradication of the indigenous infection by the end of 1985, but also
in the following years, when new infections were introduced from abroad. The results concerning the
infection in cattle and swine were comprehensive and of extreme importance, not
only for understanding the epidemiology of this particular infection but also for evaluating the possibilities of its control and elaborating adequate eradication schemes. Epidemiological
characteristics such as (1) respiratory airborne and (2) genital infection of cattle, (3)
airborne spread with air currents among swine and from swine to cattle within
herds, (4) airborne spread between swine herds, (5) correlation between
virulence of virus strains and their ability to form syncytia in cell cultures,
(6) higher risk of airborne herd-to-herd spread for syncytial virus strains,
(7) naturally occurring genital infection of pigs, and (8) long-distance
airborne spread between swine herds over 10-30 kilometers were original Danish
findings, all by this author except for the last-mentioned long-distance
airborne spread. This particular feature was a conclusion from investigations
of outbreaks introduced from herds south of the Danish-German border after
1985, i.e. after the indigenous infection had been eradicated, and after this
author had left the National Veterinary Research Institute.
This article dealing
with the principal epidemiological features of Aujeszky’s disease will naturally focus on results from Danish observations and investigations including all relevant results from other countries. The latency of the SuHV1 infection in swine is well documented, and its
significance for maintaining the infection in herds and possible transmission into other herds is well understood. It will consequently not be
dealt with here as a separate epidemiological characteristic.
2. The infection in cattle
2.1. Background
In 1965, Bendixen et al. reported on 64 outbreaks recorded in cattle since
its first appearance in 1931. Until 1964 they all occurred on the island of
Zealand. (Figure 1), and a
considerable number of affected animals could therefore be brought to the
veterinary clinic at the Royal Veterinary College in Copenhagen. In every case, that institute
had been contacted directly by the veterinary practitioner
or the National Veterinary Service and detailed information on the outbreaks
was carefully journalized.
Figure 1. Outbreaks of Aujeszky's disease in cattle in Denmark 1931-1964. Up to 1964, all outbreaks occurred on the island of Zealand (from Bendixen et al. 1965).
It is striking that the affected animals in 61 of the 64 outbreaks showed pruritus on the hindquarters. Many outbreaks in cattle have been reported without information about the exact location of pruritus, but the cases observed by Burggraaf and Lourens (1932) in 5 herds in Holland (cf. above) were associated with an anterior localization of pruritus, i.e. on head or chest. Jansen (1957), however, concluded from questionnaires returned from veterinary practitioners that most Dutch cases observed had posterior pruritus, as did animals from 3 outbreaks examined by Jansen and Kunst (1957). Rosenberger (1940) reported from 1925 to 1940 nine outbreaks in the Hanover area in Germany, most of them with posterior pruritus. Two to four animals were affected in each outbreak, and the animals showed disease practically simultaneously. Lamont (1947) referred to outbreaks in cattle in Northern Ireland, in a few of which the animals showed pruritus on the head or chest, but in most of them, pruritus was seen in the anal/vulvar region. In Sweden, Aujeszky’s disease was not seen until 1965 (Estola et al. 1965). In the first outbreak, some litters of piglets died, and several cows and heifers became infected showing head pruritus. Also in that country posterior pruritus was seen in later outbreaks in cattle (Rockborn and Hugoson 1972).
For many years
the significance of the localization of pruritus with the route of
infection was not understood, and percutaneous infection was thought to be most
likely (cf. Lamont 1947). Kretschmar,(1970) in his monograph on
Aujeszky’s disease expressed the opinion that this mode of infection
in cattle could be taken for granted and suggested that biting
insects like Stomoxys calcitrans were
responsible.
2.2. The
two-year study 1971-1973 and relevant results from later Danish outbreaks
From the point of view that the port of entry for a virus like SuHV1 was likely to be mucous membranes, this author decided in 1971 to study future outbreaks in cattle.
Three possible sites of primary infection were considered, namely the respiratory tract, the alimentary tract, and the genital tract. Unfortunately, only in a few cases did veterinary practitioners contact the State Veterinary Serum Laboratory (the National Veterinary Research Institute) before submitting material for laboratory examination, so only seldom material of interest in addition to the head or the thoracic or lumbar parts of the vertebral column necessary for the diagnosis could be examined. Results from the two years from December 1971 through November 1973 comprising 29 outbreaks were published in 1975 (Bitsch 1975a, 1975b) with results from a few selected outbreaks from 1974 and 1975 (Bitsch 1975c).
2.2.1.
Outbreaks with an anterior localization of
pruritus
It was of extreme significance that the outbreaks could be divided into two groups based on the localization of pruritus: (1) the outbreaks where affected animals showed an anterior localization of pruritus, and (2) outbreaks where animals showed a posterior localization of pruritus. In none of the herds were both manifestations seen.
In 12 outbreaks animals showed anterior pruritus. Of the 31 animals affected, 19 showed pruritus of the head and 7 on one side of the chest, while 5 showed no signs of pruritus (Table 1). Four animals without pruritus were examined virologically, and three had virus in the medulla thoracalis and not at all in brain material, and one animal had virus in brain material and samples from mucous membranes of the head, but not in the medulla thoracalis.
Table 1. Outbreaks in cattle from December 1971 through November 1973.
_______________________________________________
No. of outbreaks No. of animals affected total average_
Anterior
pruritus 12 31* 2.6
Posterior
pruritus_______ 17_______ 23________ _1.4__
Total 29 54 9
*Pruritus, in head area: 19; on chest: 7; no pruritus: 5.
Mucous membranes of the heads of 11 animals with head pruritus and one without pruritus but with brain involvement were examined for the presence of virus, and samples from eight animals were found positive: a strong indication of infection by the respiratory route (Bitsch 1975a). The virus titers were usually low, demonstrating that cells of these membranes of this species do not readily support the uptake and growth of the virus. In one of the cases, however, and in one later case (Bitsch 1975c), the titers in mucous membranes and in swabs here-from were remarkably high (approx. 102.5 TCID50 per 0.1 ml tissue or swab material suspensions).
In none of the cases from the two-year study with chest pruritus and/or medulla thoracalis involvement were lung material forwarded for examination. In an outbreak shortly after, however (Bitsch 1975c), a cow showing beginning symptoms of the disease was transported to the veterinary clinic at the Royal Veterinary College (together with the cow with head pruritus mentioned above with relatively high titers of virus in mucous membranes). This cow showed a slight itching on the right side of its chest. It was euthanized after two days of disease, and when it was skinned, the right side of the chest was found remarkably hyperaemic. Several samples collected aseptically from the lungs, using cauterization were found virus-positive (Bitsch 1975c). Later, the virus was found in lung material from another six cases in cattle and a goat, all showing chest pruritus (Bitsch 1984a). So altogether the virus has been demonstrated in the lungs of eight ruminants showing chest pruritus.
The results from
the virological examinations provided strong evidence of the facts (1) that
outbreaks with anterior localization of pruritus are due to respiratory
infection and (2) that the sites of virus entry and of pruritus are not
identical but related to a common part of the central nervous system (Bitsch 1975a). In fact, many years
earlier Hurst (1933) observed that after intradermal, subcutaneous, or
intramuscular injection of the virus (mainly into rabbits), histological
degenerative lesions could be found in the corresponding part of the central
nervous system and ganglia and that symptoms of pruritus started shortly after the appearance
of these changes. On these grounds he suggested that pruritus was not caused by
a stimulus of nerve endings but by an involvement of parts of the central
nervous system.
Figure
2. Plan of a cowhouse, where two cows received
a respiratory SuHV1 infection from pigs in a neighboring room. Arrows indicate
air currents through two windows with broken panes created by a ventilator (V). The virus was isolated from the lungs of one of the cows showing chest pruritus (Bitsch
1984a).
The
circumstances observed in the herds, where cattle showed an anterior
localization of pruritus, were in full accordance with this conclusion of a
respiratory infection mode (Bitsch 1975b). Practically always were
the cattle housed together with swine, most often feeder pigs, although not in
close contact with them. Three different situations could be
observed: (1) if the room was equipped with a ventilator expelling the air, the
affected animals were typically placed between the ventilator and the pigs; (2)
if there was only a simple air duct in the ceiling without a fan, affected
animals were often placed close to the air duct with pigs just opposite, as if
the air had circulated around the duct before leaving through it (like water
let out of a sink or a bathtub); and (3) if there were no ventilation
installations in the room, cases in cattle might appear almost everywhere. A special situation was seen in two later
outbreaks, where the source of infection obviously was feeder pigs in an
adjacent room: in one case there was a permanent aperture in the separating
wall, while in the other one (Figure 2) the wall was supplied with
windows, where some panes were broken (Bitsch
1984a). The affected animals, five and two, respectively, were placed just
between these wall openings and ventilators, which were found to expel
air from the rooms with swine through the apertures described. On average, 2.6 animals were infected in each
outbreak. In one of the herds, however, where the shared cattle and swine house
was poorly ventilated, an outbreak had occurred one year earlier affecting 14
head of cattle. In none of these outbreaks did the animals show a posterior
localization of pruritus, and in no case was a transmission of the infection
among cattle found likely to have occurred. However, the finding of relatively high
virus titers in mucous membranes or swabs here-from in the few cases mentioned
above may be taken to indicate that cattle-to-cattle transmission may occur occasionally.
The duration of
clinical disease is shorter in animals with a head involvement than in animals
with a lung infection. Typically the first group died after approximately 24
hours, while the second group showed symptoms for a couple of days (Bitsch 1975a).
Sufficient evidence has been
accumulated for the following conclusions concerning outbreaks of Aujeszky’s disease in cattle with an
anterior localization of pruritus:
1. Cases regularly result from respiratory infection.
2. Cases with
head pruritus are associated with primary infection of mucous membranes of the
nasal or pharyngeal cavities.
3. Chest pruritus is associated with a primary lung infection.
4. Primary infection of the upper and lower respiratory tract may proceed without
signs of pruritus.
5. Animals
infected by the upper respiratory tract typically die after one day of disease,
while
animals suffering from lung
infection show symptoms for approximately 2 days.
6. Individual cases in cattle regularly receive the infection airborne directly from swine.
7. Respiratory Aujeszky’s disease is a dead-end infection in cattle.
8. Animals at risk are those exposed to air currents from pigs infected by the respiratory route.
9. The site of
pruritus, iatrogenic cases disregarded, is not the site of virus entry. Still, those two
sites are related to a common part of the
central nervous system, most probably also involving
sensory ganglia. Pruritus in Aujeszky’s disease thus appears to be a neurological condition due
to damage or stimulation of the central nervous system, and the intense
itching of a skin area
must be considered a phantom sensation.
2.2.2.
Outbreaks with a posterior localization of
pruritus
In 61 of
the 64 outbreaks occurring from 1931-1964 reported by Bendixen et al. (1965), all 114 infected animals showed a posterior
localization of pruritus. In 60 percent of these, only one animal was
infected, the average number being 1.7. In two herds, cases appeared at
a one-year interval, and in a third herd, an outbreak reappeared after 5 years.
For 16 affected calves under one year of age, their sex was not recorded, but
the remaining 98 animals were all females. The cattle and swine herds were
relatively small. In 39 cases the veterinary practitioners had informed about
the size of the swine herd. All had sows, and 19 herds informed about the regular use of boars from boar centers for natural service. From the size of the swine herds, however,
the authors judged that such boars had regularly been used in the large majority
of the herds.
In the material
from the two-year study, 17 of the 29 outbreaks were associated with
posterior pruritus (Table 1). Again,
most often only one animal was infected in each outbreak, the average number
being as low as 1.4. If more than one animal was infected, they
usually showed symptoms on the same day, in a few cases up to two days apart (Bitsch 1975a). One outbreak deviated
from the rest by the finding that the infection had obviously been transmitted
by the veterinary practitioner, just as it was also found in a few later cases
(Bitsch 1975c). This outbreak was on
a farm with cattle and a big swine herd. The remaining 16 outbreaks
all occurred on farms with small swine herds and in none of these herds were
symptoms of the disease in swine observed. Of special interest was that the
affected animal on one farm was a bull calf. Samples were collected from the rectum
and several sections of the intestines of that calf, but no virus could be
found (see later). Only in three
cases from two herds were vaginas received for examination, but the virus was found
in all three of them, although at low titres. Veterinary practitioners were
therefore encouraged to contact the laboratory before forwarding material for
examination, and over the following years, vaginal samples from a further 22
animals from 21 outbreaks were found virus-positive, while vaginal samples from
14 animals from 13 outbreaks were found virus-negative (Bitsch 1984a).
Generally, however, the titers demonstrated in vaginal samples were very low,
indicating that a negative result did not exclude vaginal
infection. These additional results show that in the majority of
outbreaks in cattle with a posterior localization of pruritus, animals are
infected by the vaginal route. It was
characteristic that there were relatively few sows in the herds
and that boars from boar centers had been used for natural service of the sows.
(More details are given below in the section on genital
infection in swine).
Animals showing
pruritus on the hindquarters typically die after 2 days of disease just as the
animals suffering from lung infection (Bitsch
1975a).
In one case from
the two-year study (Bitsch 1975a,
1975b) and three later cases (Bitsch
1975c) the findings indicated iatrogenic
infection. Two of these animals showed pruritus on their hindquarters,
while the remaining two showed pruritus in the flank area, in one of them
involving a surgical wound.
The possibility of alimentary infection was left open after the early studies 1971-1973, especially because of the case in a bull calf mentioned above, most probably being the only natural case ever in a male bovine animal with posterior pruritus1. Alimentary infection of cattle must now be considered unrealistic.
[1] The farmer's
wife explained that this calf was their special pet animal. It was not tied up and followed persons
around in the cowhouse like a dog.
The conclusions concerning cases in cattle with a posterior localization of
pruritus are therefore:
concerning cases in cattle with a posterior localization of pruritus are hereafter:
1. Cases have regularly been associated with vaginal
infection. The vagina must accordingly be
considered the port of virus entry.
2. Clinical disease typically lasts two days.
3.
Outbreaks have regularly occurred in combined swine and cattle herds, where
boars from boar centers have been used for natural service.
4. Generally, one or two animals are infected in each outbreak.
5. If several animals are infected, they usually
become infected at the same time.
- A center boar regularly served a sow 5-8 days before symptoms.
- Some extreme cases have been iatrogenic.
- Cases have never been reported associated with observed clinical
disease in swine.
- Percutaneous infection is unlikely except in iatrogenic cases.
- Alimentary infection is not a realistic possibility.
3. The
infection in swine
3.1. Pathogenicity
of virus strains
3.1.1. Syncytial
and non-syncytial virus strains
SuHV1 exhibits a virus
strain-specific cytopathogenic effect (CPE) in susceptible tissue cultures of
mainly two types: where the infected cells (1) form syncytia (syncytial virus
strains) or (2) become rounded or ballooned (non-syncytial virus strains), cf. Kaplan 1969. All cases in cattle in Denmark up to 1964 occurred on the island of Zealand (Figure 1). But in 1964 three outbreaks were diagnosed in Jutland. The
structure of the swine production was changing. From 1950 to 1964 the annual
number of pigs slaughtered gradually rose by 300 percent (Bendixen et al. 1965), and this tendency continued over the
following years. Conventional breeding herds and herds with specialized
production of fattening pigs became steadily larger.
In Denmark, as in many other countries in Europe,
Aujeszky’s disease was not seen as a disease problem in pigs until many years
after its clinical appearance in cattle. The first Danish outbreak in swine was
seen in 1964 in Zealand (Andersen et al. 1964), and over the next
years, the infection was spread rapidly, especially in Jutland (Figure 3) (Bitsch
and Andersen 1982, Bitsch 1983). But clinical
symptoms other than fever were seen only in piglets, and generally only litters
under two weeks of age were clinically affected. On average, two litters died
in each outbreak.
In the 1970's the situation changed further, when more severe outbreaks appeared in especially big herds. Whole litters over 2 weeks of age died as might also older pigs, and sows were
seen to abort infected fetuses.
This
new situation with more severe respiratory disease in pigs was reflected also by a higher frequency of outbreaks in cattle with an anterior localization of pruritus caused by respiratory infection (Figure 4).
Figure 4. Outbreaks of Aujeszky's disease in cattle in Denmark 1968-1983.
Note the increased number of outbreaks with anterior pruritus associated
with the appearance and spread of syncytial virus strains after 1979.
At the same time, it was observed that the higher degree of
pathogenicity of the virus isolates could be related to their cytopathic effect
(CPE) in tissue cultures. Virus isolates from cattle with
pruritus on the hindquarters were consistently non-syncytial, while most isolates
from cases with anterior pruritus were syncytial (Table 2), but also isolates from severe outbreaks in swine herds were - in contrast to isolates from most other outbreaks in swine - found to be
syncytial (Bitsch 1980[1].
In the following years, syncytial strains became the predominating isolates (Figure 5), especially from big herds in Jutland (Bitsch and Andersen 1982, Bitsch 1983, 1984a). This correlation between virulence and type of CPE was later found also in other countries. Harkness and Sands
(1985) found concording results with British isolates and a series of coded
virus isolates from Northern Ireland received from J.B. McFerran examined by this author gave similar results[2]. The highly virulent virus strains introduced by the airborne mode
into Denmark from herds south of the Danish-German border after 1985 were all found syncytial (see later).
Table 2. Prevalence of syncytial and non-syncytial virus in Aujeszky's disease cattle up to 1980 (Bitsch 1980) _________
No. of Type of virus
strain involved outbreaks* syncytial non-syncytial
Anterior
pruritus 17 14 3**
Posterior
pruritus______ 25______________ 0 25***_
Total 42 14 __ _ 28____ _
*Isolates from all 29
outbreaks in 1978 and 1979 were supplemented with isolates from 1972 to 1977.
**Only one animal was
infected in each of these three outbreaks.
***All isolates from the many later outbreaks of this type were also
non-syncytial.
_______________________
[1] Of the isolates from swine
evaluated, four were judged to be of an intermediary type. For practical
reasons, they were later included
among the non-syncytial strains.
[2] The CPE produced by one of the isolates, the NIA 4 virus strain of obscure origin and similar, if not identical, to the Hungarian Bartha vaccine strain, showed a CPE clearly uncharacteristic of herpesviruses.
3.1.2. Restriction
fragment pattern analysis of virus DNA
It was evident from the results in 1978 and
1979 that Aujeszky’s disease had become a more severe disease over the last few
years. This was the main reason for the decision in 1980 to control and
eradicate the infection. An important question was the origin or the cause of
the new more virulent strains. In this context it should be noted that import
of swine had been prohibited for many years up to 1972, when Denmark joined the
European Common Market, most probably to protect the Danish landrace from foreign
genes, and after 1972 all animals imported were subjected to control of
Aujeszky’s disease, both before import but also after a quarantine period as
required by the farmers' organizations. So infected pigs had not been
imported for decades.
Gielkens and Berns and Ludwig et al. reported in 1982 on the differentiation of SuHV1 virus isolates using restriction fragment pattern analysis of the virus DNA. A.L.J. Gielkens agreed to test some Danish isolates receiving four isolates: a syncytial respiratory and a non-syncytial genital strain from cattle, and a syncytial and a non-syncytial respiratory strain from swine, all from outbreaks in 1982. He responded immediately (May 1982) with the information that the four isolates appeared identical but differed from all other European strains, he had tested so far. One characteristic difference was that fragment/band 9 from the BamHI analysis of the Danish isolates was missing. These results were published in a later report (Gielkens et al. 1985).
H. Ludwig received a syncytial respiratory strain from swine
and a non-syncytial genital strain isolated in 1981 from cattle and found them
to be identical to a Danish cattle isolate from1962 (posterior pruritus) and a
Swedish pig isolate from 1982, but again different from all other SuHV1 strains
investigated (Herrmann et al. 1984). They found that European isolates could be
divided into three major groups, which were designated I, II, and III. Group III comprised exclusively the Danish-Swedish strains. Todd and McFerran (1985) tested two syncytial and two non-syncytial Danish isolates, one of which was the first genital isolate directly from pigs, from 1980 and 1981 with identical results. Christensen and Sørensen (1988) tested
approx. 70 Danish isolates which all, apart from six isolates from herds
infected within one month in the winter of 1985 in an area not far from the
German border (Figure 6, cf. section
on airborne transmission), were found to be Group III strains.
Figure 5. Outbreaks of Aujeszky's disease in pigs 1978-1983 by syncytial and non-syncytial virus (Bitsch 1984a). In 1985 there were 38 outbreaks, of which 32 (84%) were caused by syncytial strains (cf. Figure 6).
The important conclusion made in 1982 after the response from A.L.J. Gielkens on his preliminary analyses that the new virulent Danish strains had not been introduced from abroad but had developed from Danish strains of lower pathogenicity (virulence) was in this way substantiated by the results from many later investigations.
In summary, the main conclusions concerning the degree of pathogenicity (virulence) of SuHV1 strains are:
1. Syncytial virus strains a higher degree of pathogenicity to both cattle and swine than non-syncytial strains.
2. Isolates from cattle exhibiting posterior pruritus (iatrogenic cases not considered) are regularly non-syncytial.
3. SuHV1 appears to vary in degree of pathogenicity. Over time, the virus may become more virulent along with changes in the pig breeding and production structure.
4. Danish virus strains are unique and constitute a separate group of SuHV1 viruses. No foreign strains were introduced into Denmark before 1985.
5. Danish virus strains are unique and constitute a separate group of SuHV1 viruses. No foreign strains were introduced into Denmark before 1985.
6. Changes in virulence occurred in two major steps. The first step was the establishment about 1964 of respiratory virus strains from genital strains, which were spread vigorously over the following years causing outbreaks in pig herds and the death of piglets a few weeks old, and the second step was associated with the development and spread in the 1970's of the more virulent syncytial, respiratory strains.
7. The ability of a SuHV1 isolate to cause syncytium formation in cell cultures is a valuable characteristic or marker of virulence.
3.2. Airborne transmission within and between herds
The results from the study of Aujeszky’s disease in cattle referred to above demonstrated clearly, not only that cases in cattle exhibiting pruritus on the head or chest were due to respiratory infection, but also that the individual cases received the infection directly from swine in practically all instances. At the same time, it was illustrated that virus from respiratorily infected pigs was carried away by air currents over relatively long distances, not even to animals in the same room, but also in some instances to animals in adjacent rooms (Bitsch 1975a, Bitsch and Andersen 1982, Bitsch 1984a). Transmission of an infectious agent by air currents was demonstrated clearly. The spread among pigs of a respiratory virus like SuHV-1 with a diameter almost 10 times that causing foot and mouth disease and acknowledged to be spread airborne, was thought to require close or relatively close contact between individuals. However, the findings with Aujeszky’s disease in cattle, which were relatively resistant to infection by the respiratory route, implied that the predominating or decisive spread among swine in ventilated rooms would be by air currents over many meters rather than transmission among animals in close contact. Furthermore, the ventilation system would send considerable amounts of virus out into the surroundings exposing other herds to a risk of infection.
Donaldson et al. (1983) demonstrated under controlled experimental conditions that a respiratory virus could be sampled from the air in loose boxes with infected animals and that infection could be transmitted by air from infected pigs in one box through an air duct to uninfected pigs in another box.
The Danish observation that air containing considerable amounts of virus was moved by ventilators and blown out into open air furthermore implied that the infection might also be spread by the airborne mode to swine farms in the surroundings. The risk of infection for other herds would naturally depend on (1) the effect and construction of the ventilation system (2) the size of the infected herd as well as that of those at risk, (3) weather conditions, (4) length of time of exposure for herds at risk, (5) characteristics of the virus strain and (6) distance from the source of infection. After the appearance of syncytial virus strains (Bitsch 1980) a growing number of especially closed big herds became infected. Some cases concluded to have been caused by airborne virus transmission were described by Bitsch and Andersen (1982), and others later (Bitsch 1984a). Transmission had been noted to occur over distances of up to 3 kilometers. In one of the early cases, where an SPF herd was concluded to have received the infection from a large herd with sows and fattening pigs 500 meters away, the air blown out by ventilators of the latter could actually under certain weather conditions be followed over considerable distances as relatively thin “wisps of smoke”.
Figure 6. Outbreaks in swine herds 1985.
Symbols: Encircled
dots: 6 outbreaks caused by
non-syncytial strains.
Triangles 32 outbreaks by syncytial
strains.
The
6 outbreaks close to Germany were by a foreign syncytial strain.
In 1984 Gloster et al. reported on the
possibility of airborne herd-to-herd spread of Aujeszky’s disease between herds in Yorkshire and concluded that meteorological and
epidemiological data suggested that airborne transmission might have occurred
in some of these cases.
In 1987 Christensen et al. reported on
restriction pattern analyses of virus DNA from all isolates of SuHV1 from 1985 (cf. Figure 6). The analyses were extended in a subsequent paper (Christensen and Sørensen 1988) referred to above in the section on the pathogenicity of SuHV1 strains. The main finding was that all Danish
isolates - apart from those from six outbreaks in swine
herds in the south of Jutland, which occurred early in 1985
within one month - belonged to Group III of the SuHV1 virus.
Virus of this group has been recovered only from outbreaks in Denmark and
Sweden, cf. above. The six deviating isolates were Group II viruses and were
from herds situated within 10 kilometers of each other. It was concluded that
the primary source of infection for
these six herds was herds south of the Danish-German border[1].
As seen in Figure 6, the outbreaks in 1985 caused
by syncytial virus appeared in clusters, which was due to airborne spread of
the infection among the herds.
In two later
papers (Christensen et al. 1990, Christensen et al. 1993) was reported on
introductions of
Aujeszky’s disease virus identified as various subtypes of
group II viruses into Denmark in the winters of 1986/1987, 1987/88, 1988/89 and
1989/90. On basis of comparison with isolates from Northern Germany, and of
meteorological data and other special conditions it was concluded that the
infection had been transmitted by the airborne mode from German herds to some
Danish herds in the south of Jutland, from where it was further spread
similarly to other herds. In the winters of 1987/1988 and 1989/90, it was even
spread more than 30 kilometers over waters to the island of Funen[2].
________________________
[1] All isolations of SuHV1 from outbreaks in 1985 were made by this author, and these isolates together with earlier isolates were forwarded to the Danish Veterinary Virus Research Institute by the end of 1985 for further investigations. Unfortunately, in the two papers giving the results (Christensen et al. 1987 and Christensen and Sørensen 1988) it is erroneously mentioned that one of the six isolates differing from the traditional Danish virus strains originated from a herd in the mid-part of Jutland. But all six deviating isolates were from herds situated in a small area in the south of Jutland, cf. Figure 6.
[2] Another respiratory disease of domestic animals,, infectious bovine
rhinotracheitis, IBR, by Bovine herpesvirus
1 was eradicated in Denmark from 1984 to 1991. During the eradication period, several acutely infected herds were concluded to have received the infection
by airborne mode from a neighboring acutely infected herd. And already in the winters of 1990 and 1991, some
new infected herds close to the German border were concluded to have been infected from herds south of the
border. But also in the years 1992 to 1995 and in 2001 after the final eradication in herds in the
border county were found infected in the winter period. Airborne transmission from German herds was
concluded to be the only possible explanation. Most infected herds were situated within a few kilometers from the border,
but two were 10 and 25 kilometers away. In some instances, neighboring herds got infected subsequently. In
one particular case, a dairy herd 300 meters from an infected herd showed a low reaction in bulk tank milk shortly
after the outbreak, but only one animal had gotten infected in this herd. Of special interest was that this cow
was placed in the cowhouse just between a ceiling ventilator and air intake in the wall
facing the infected farm. The risk of airborne herd-to-herd transmission of IBR is considerable, although not of quite the same
magnitude as the risk of herd-to-herd spread of syncytial strains of SuHV1. The investigations were performed by this author.
_____________________
The most important conclusions related to airborne
transmission of SuHV1 are hereafter:
1. Within
a herd the decisive transmission of the respiratory virus will follow air
currents over
many meters, in ventilated rooms determined by the ventilation
system. Spread from close
animal-to-animal contact will generally be of minor importance.
2. The risk of herd-to-herd transmission will be high in areas with big swine herds with
effective ventilation systems. An infection may be spread over distances of
many kilometers.
3. Syncytial
virus strains are more likely to be spread by the airborne mode than are
non-syncytial respiratory strains.
3.3. Genital
infection of pigs
Aujeszky's
disease in cattle showing pruritus on the head or chest is due to respiratory
infection. After the appearance of
the highly pathogenic, syncytial virus strains, such outbreaks become
predominating (cf. Figure 4). But up
to 1964, the large majority of the outbreaks in cattle was associated with
pruritus of the hindquarters. In later such cases, the virus was demonstrated,
although in low titers, in the vagina of
most of the animals examined, and the obvious conclusion was that the vagina
was the port of virus entry (cf. Section
2 above). But still, up to 1980, the way of transmission from infected
swine remained to be demonstrated. The fact, however, that cases regularly
appeared in small herds using centre boars for natural service (at least in
Denmark and Sweden, where this particular characteristic had been observed)
made it logical to anticipate that these boars had introduced the infection to
sows in a genital form.
Akkermans (1963) (see also Akkermans 1964) tested 40 boars aged 6 months to several years from boar centers in the
Netherlands. He concluded that they originated from uninfected herds and found
that practically all had become antibody-positive by the age of one year. Furthermore, a boar was infected nasally with a respiratory strain whereafter the infection was transmitted to the vagina of
two sows served 6 and 16 days later, although preputial swabs consistently were
virus-negative. In another experiment, a sow was infected by the vagina using
the same virus strain. Virus was demonstrated in vaginal swabs for 8 days, and
after four days she was mated with a boar, after which the virus could be found in
preputial swabs from this boar for nine days. However, no genital strain was
used in the experiments, so no particular conclusions can be made from these
results. Natural genital infection has never been demonstrated
in the Netherlands.
In 1967 in Sweden, Rockborn and Hugoson (1972) noticed in a herd with Aujeszky's disease in a cow that a center boar had visited the herd two
weeks earlier. Of 9 boars from the center, 5 were found antibody-positive. Sows
from herds, where boars from that center had been used, were then blood-tested
at slaughterhouses in 1968. Of 424
sows from 149 herds, 123 (29%) from 64
herds (45%) were found antibody-positive. No clinical signs of the infection
had been seen in pigs in these herds.
The close
correlation between outbreaks in cattle and the use of center boars was reported
already by Bendixen et al.
(1965). The first 60 outbreaks up to
1964 all occurred on the island of Zealand (Figure 1). In early 1984, one-third of boars from boar centers on that
island were found serologically positive, and when small herds in the area were
tested, a usual finding was single reactors among the sows.
Demonstrating
porcine genital infection was attempted in 5 outbreaks (Bitsch 1984b, Outbreaks 1 to 5), the first time (Outbreak 1) in
1981. A sow had been served by a center boar (Day 0) before the appearance of disease symptoms in two calves (Day 5). The virus was demonstrated in the vagina of both calves and also in a vaginal swab
collected on Day 7 from the sow at a titer of 106.2 TCID50 per ml of the swab fluid (further details of
this outbreak are given in Section 4).
In an outbreak
from 1983, where the virus was demonstrated in the vagina of a cow (Bitsch 1984b, Outbreak 4), the virus was
found in a vaginal swab collected from a sow served by a center boar close to
one week before the death of the cow. The virus titer was 105.5
TCID50 per ml swab fluid. The affected cow was reported to be in oestrus on
the day of insemination of the sow (cf. suspicion of sodomy, Section 4). In an outbreak from 1982 (Bitsch 1984b, Outbreak 3) a sow (Sow 1)
had been served by a center boar on November 15 (Day 0), and a cow showed
clinical disease on Day 15. There were only 2 sows on the premises, and vaginal
swabs were taken from these and the cow on Day 17. The samples from Sow 1 and
the cow were negative, while the sample from the second sow showed a virus
titer of 10.3.5 TCID50 per ml of the swab
fluid. Unfortunately, only the lumbar spinal cord and not additionally the
vagina of that cow was forwarded to the laboratory for examination. The boar
mentioned was the only contact with swine from other herds for several months,
and a logical conclusion was that virus had been transmitted from the vagina of
Sow 1 to the other sow and the cow at practically the same time approximately
one week after the mating of Sow 1 (for more details, see Section 4).
In a further two
outbreaks (Bitsch 1984b, Outbreaks 2 and
5) vaginal swabs from sows were
examined virologically, but with a negative result. In Outbreak 2 from 1982,
two heifers showed clinical disease on February 23, and the virus was found in the
vagina of the one examined. Two sows had been served by center boars 7 and 11
days earlier, but vaginal swabs taken from the sows five days after the
clinical outbreak, i.e. 16 and 12 days
after service, respectively, were found negative. In Outbreak 5, where a calf
showed signs of Aujeszky's disease on September 19, 1983, virus was found in
the vagina of the calf. Vaginal swabs collected from two gilts, which had been
served by a center boar nine days before disease in the calf, were found
negative, but the sampling was not performed until 12 days after service. Blood
samples, however, taken of both of them showed low antibody titers. Apart from the gilts, there were
only some feeder pigs in this herd. So, for these two outbreaks, it
must be concluded, that although vaginal infection was most likely introduced
as a genital infection approximately one week before the disease in cattle,
the samples from the sows had not been collected early enough, as the
development of antibody will hamper virus recovery after more than one week.
The main
conclusion from the investigation of the five outbreaks reported in 1984, where
center boars were suspected of introducing the infection, was that the genital infection could be confirmed in sows in three of them while in the remaining two, samples were collected too late for
confirmation of the expected vaginal infection of the sows. The results closely
linked cases of Aujeszky's disease in cattle with pruritus on the hindquarters
to genital infection in swine on the same premises. At the same time, they convincingly documented
two special epidemiological features of Aujeszky's disease in pigs, namely (1) the natural occurrence of a true porcine genital infection and (2) the spread of this
manifestation of infection between swine herds by center boars used for natural
service.
Romero et al. (1997) subjected naturally
infected wild pigs in the USA to immunosuppression using dexamethasone and
isolated SuHV1 primarily from the vagina and prepuce and less frequently from
the respiratory tract of these animals.
When 6 naturally infected boars were placed together with 5 uninfected
and non-pregnant gilts and were examined over eight weeks, virus could be
demonstrated in vaginal samples, but not in nasal swabs from any of the
animals. In a later experiment (Romero et
al., 2001), infected
non-pregnant sows were kept with uninfected boars for six weeks and virus
could be demonstrated in preputial swabs and not in nasal swabs from the boars.
Likewise, when infected boars were kept together with uninfected gilts, virus could be found in vaginal swabs and not in nasal swabs taken from the gilts. Their conclusion was that the SuHV1
infection in wild pigs was primarily maintained as a venereal infection.
According to
various web sources, wild pigs in the USA were originally escaped domestic swine. About a century ago, however, wild pigs were imported into the USA from
Europe, and the wild pigs today are a mixed breed
population. It is noteworthy that the
SuHV1 infection appears to occur in wild pigs in the USA in the form that was
prevailing in domestic swine in Europe before the development and intensive
spread of the respiratory strains
The main conclusions related to yhe
occurrence of porcine genital infection with SuHV1 are hereafter:
- Genital infection is a specific
epidemiological entity of the infection.
- It has been maintained in domestic swine in many countries for long periods by center boars used for the natural service of sows in different herds.
- It has always been asymptomatic in infected pigs.It has always been asymptomatic in infected pigs.
- Indications of respiratory spread of an infection introduced in a venereal mode have never been observed.
- The many genital isolates from swine and cattle in Denmark have consistently been found to be non-syncytial, and there is no reason to suspect that this should not account also for genital strains from other countries.
- The natural genital infection has been demonstrated also in wild pigs.
4. Selected outbreaks in cattle with a posterior
localization of pruritus: supplementary details pointing to the involvement of
animal sodomy (zoophilia/bestiality) in the transmission of the infection
Sodomy is a
delicate subject, so when investigating outbreaks, it will be unacceptable to
suggest a such action to have taken place, also to the local veterinary
practitioner. Relevant information therefore had to be collected indirectly and
with much care. Naturally, the most valuable sources of information were the
farmer or his wife and their practicing veterinarian.
The first
outbreak, where sodomy was found likely to have been involved, also was the
first case ever, where the virus was demonstrated in the vagina of an affected
bovine animal (Bitsch 1975b, Outbreak
14). The farmer had brought a sow to a boar center for service about 5 days
before the disease appeared in the calf. From the veterinary practitioner, I
learned (1) that the owner was a bachelor and (2) that he - early in the
afternoon, shortly after having returned home from the center – had brought the
affected calf in from the field and placed it in the house next to the sow,
where it remained until it got sick. When talking to the farmer I suggested
that he might have gotten his hands contaminated by pulling the tail of the sow and that he thereafter by dragging the calf by its tail might have transferred the virus to the perineal region. But the farmer did not respond at all hereto.
A second
outbreak was the very first case of proven naturally occurring genital
infection in pigs (Bitsch 1984b,
Outbreak 1). Fortunately, the practitioner phoned to me early about two
suspected cases of Aujeszky's disease in calves showing posterior pruritus.
Without hesitation, I then told him (1) that the two calves would be females,
(2) that they would be placed next to each other and that the neighboring
calves would be males, and (3) that a sow would have been served by a center
boar approximately one week earlier. He immediately confirmed the two first
postulates. In fact, 11 calves were stalled in a row, where No. 2 and No. 3 -
the affected ones - and No.10 were females, while the rest were males. He
promised to forward the vaginas of the calves and a vaginal swab from the sow for laboratory examination. The virus was found in both vaginas, and a high
virus titer was demonstrated in the vaginal swab from the sow, cf. Section 3.3. According to the farmer's wife, sows to be
served were usually pointed out to the one bringing the boar by herself or her
husband, but in this particular case, they had both been away and had been
substituted by their son. According to the practicing veterinarian, their son
was “15 years old or so”. When the boar had left, their son was quite alone at
home.
In a third case
(Bitsch 1984b, Outbreak 3) I was first contacted by the practitioner, who reported that a cow in a herd had shown
symptoms of Aujeszky's disease with pruritus in the tail region. I then responded that a sow in the herd would have been served by a center boar about a week
earlier, and asked him to collect a vaginal swab from that sow for examination.
However, at the farm, he phoned back and told me that the sow (Sow 1) had been
served two weeks earlier. There were only two sows on the premises, so he agreed to
take a vaginal swab also from the second sow (Sow 2). The vaginal swab from Sow
1 was found negative, as expected because it was collected too late after
service. But the vaginal swab from Sow 2, which had not been served recently,
showed a relatively high virus titer (see Section
3.3). It appears unquestionable that the infection originated from the
boar, but the virus had not been transmitted to the cow shortly after the mating.
Actually, the findings were consistent with a transmission of the infection
from the vagina of Sow 1 to the vagina of Sow 2 and the affected cow
approximately one week later. In this respect it is of interest that Sows 1 and
2 were housed in a separate building, while the infected cow and other bovine
animals were in the cowhouse on the other side of the farmyard. The center boar had been the only contact
with swine from other herds for several months.
In a later
outbreak, we came as close to a confession of animal sodomy as one can get
without using that particular term. The virus was found in the vagina of a heifer,
which was placed immediately next to the sow served a week earlier by a center
boar. When I phoned the farmer some days after the delivery of the laboratory
results, I got into contact with his wife. I explained to her about the
situation: that virus would have been introduced by the boar, and that the
heifer would have received a vaginal infection. Furthermore, I suggested that if
a person later that day had brushed the hindquarters of the sow and then in
immediate succession with the same brush also the tail region of the heifer, I
would realize a risk of transmission of the infection to the heifer. I then heard her speak to someone in the
room, saying: “Peter (name changed), it is the laboratory veterinarian. He
tells me, that if one has brushed the hindquarters of the sow and
thereafter the hindquarters of the heifer, one may have transmitted the
infection from the sow to the heifer. I saw you were out there in the evening.
The lights were on”. I could not hear the other person speak, but after a while, she returned and said shortly: “I was speaking to our assistant. He tells me
that he has done so”. It was striking
that she did not hesitate at all. She knew immediately which day the sow had
been served, and that the lights had been on in the animal house in the evening
on that particular day. Most probably,
she and her husband had already talked about what might have taken place. And
that the assistant that evening should have brushed the hindquarters of those
two animals is definitely unlikely.
Finally, one
particular outbreak deserves to be mentioned. A cow and her calf, both showing
posterior pruritus, died close to one week after delivery of the calf. We
demonstrated the virus in the vagina of the cow, but the calf was not examined.
When I later visited the farm, I inspected the farm buildings together with the
owner and his young male assistant. In the barn there was in one corner a pen
with a sow, which had been served by a center boar some days before the appearance
of the disease, and in another one a
calving box, where the cow had been with her calf. There were no other
animals in that room.
As mentioned
earlier, one or two animals were usually
infected in each outbreak with posterior pruritus, which fits with the notion
of involvement of sodomy. But in extreme
cases, several more animals have been infected. Shope (1931) mentions an outbreak, where 9 animals showed pruritus
on the hindquarters. Bendixen et al. (1965) informed of an
outbreak with 7 cases and in a later Danish outbreak even 10 cows got infected.
But from the details of this last outbreak given in the footnote below, it will
be seen that also here sodomy may very well have been involved.[1]
Concluding remarks on sexual
transmission of SuHV1 from swine to cattle by man:
Although animals in the first
outbreaks in cattle in European countries (Aujeszky 1902, Bang 1932, Burggraaf and Lourens 1932)
showed pruritus on the head or chest (respiratory infection, cf. above), the manifestation associated
with pruritus on hindquarters was predominating in cattle in Europe for many years. The port of
virus entry and the way of transmission of the infection from swine to cattle remained obscure. One
step forward in the understanding of these questions was the finding that viral vaginal infection could
readily be demonstrated in most of the bovine cases. Another feature was that cases were linked to using center boars for service of sows in the
herd and vaginal infection of a sow. The virus could be demonstrated in the vagina of a sow if not tested later than the time of death of the bovine animal. The. evidence that the
genital infection in sows had been sexually transmitted to the cattle by man must be considered substantial, as all findings are consistent with that explanation.
[1] Unfortunately, the
laboratory was not contacted during that acute outbreak, and just lumbar CNS material of one cow was received
from an incineration plant several days after the outbreak. The animals got
sick at the end of one week. Later, we received detailed information from the
veterinary practitioner about the onset of the disease, the time of death of the individual animals, and their location in the animal house, where 34 dairy cows, calves, and pigs were housed. According to the farmer's wife, a center boar had served a sow the
preceding Saturday. When I later phoned the farmer to learn if pigs had been loose in the house that particular weekend, I talked with
his daughter, who explained that to their knowledge no pigs had been loose. However, they still needed to ask her brother, because that weekend he had been home on leave from military service and that Saturday evening,, he had been the only one at home.
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