Download Myxomatosis in France

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Myxomatosis in France
Overview
Following the dramatic spread of
myxomatosis in Australia early in 1951, an
illegal introduction for rabbit control was
made on an estate near Paris in June 1952.
The strain of virus used (‘Lausanne’) was
recently derived from its Sylvilagus host in
Brazil. It led to the establishment of the
disease in France. Over the next decade
myxomatosis spread to most of the
countries of Europe in which rabbits are
found, producing very high mortalities.
The public reaction to myxomatosis in
France was dominated by deep concern by
rabbit breeders for the safety of their
domestic rabbits and by chasseurs for the
destruction of an important hunting
animal, the wild rabbit. On the other hand,
foresters and most farmers welcomed the
destruction of a major pest. Vaccination of
domestic and wild rabbits was practised
on a large scale.
The Lausanne strain was highly lethal
and the skin lesions were much more
protuberant than those produced by the
virus used for the Australian introduction.
Less virulent strains were recognized two
years after its introduction, and tests nine
and fifteen years later showed that a
variety of strains of differing virulence
were present, the percentage of highly
virulent strains decreasing progessively to
2% by 1962. In 1980 a ‘non-myxomatous’
or ‘respiratory’ form of myxomatosis was
observed in commercial rabbitries; it soon
became the commonest form and was
thought to be transmitted by close contact.
Initially the populations of wild rabbits
were decimated, and even with the reduction in virulence of the virus and the
increased resistance of the rabbits, by the
1990s myxomatosis appeared to have
produced reductions in the wild rabbit
populations to somewhat less than half
those found before 1953.
Introduction into France
The dramatic outbreak of myxomatosis
among rabbits in Australia in early 1951
received extensive media coverage in
Europe. The first international responses to
this demonstration of its effectiveness for
rabbit control occurred in France.
Enquiries from the Institut Pasteur, Paris,
January 1952
On 22 January 1952 Dr G. Remaudière, of
the Service de Parasitologie vegetale of the
Institut Pasteur, wrote to Francis Ratcliffe,
the head of the Wildlife Survey Section of
CSIRO, requesting reprints on myxomatosis,
a specimen of the virus and details on its
cultivation, and saying, amongst other
things1:
Les lapins constituant dans certaines parties
de la France, un véritable fléau, l’Institut
Pasteur désirerait entreprendre la lutte
biologique contre ce Rongeur et essayer de
développer une épidémie de myxomatose en
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Sologne. Cette région infestée de lapins
semble, à priori, favorable à l’expansion de la
maladie, car les Culicides et Simulides sont
abondants.
Ratcliffe passed the letter to his
colleague Fenner, who on 15 February 1952
sent Remaudière two vials of freeze-dried
myxoma virus and full particulars of the
method of preparation of large quantities
for inoculation campaigns. Receipt of the
letter and virus was acknowledged on 29
February, but no further information about
the use of the virus was received in
Australia or could be found in a recent
search of archival sources in France.
Release of myxoma virus on Maillebois
Estate, June 1952
Dr P.F. Armand Delille (Fig. 9.1) was a
distinguished physician and bacteriologist
who was 77 years old when he read in the
Paris papers of the great epizootics of
myxomatosis in Australia in 1950–51, and
conceived the idea of eliminating wild
rabbits from his estate at Chateau Maillebois
(Eure-et-Loire) by the use of this virus.
Lockley describes his visit to Maillebois in
December 1953 in the following terms
(Lockley, 1964):
At that moment Dr Delille was a very worried
man; proceedings against him had been
begun by hunting and sporting interests in
France, and he was engaged with his legal
advisers in Paris preparing to defend his
actions in the law courts. A test case was
being brought against him, with the financial
backing of the hunting clubs of France, by the
local owner of a domestic rabbitry in which
the rabbits had all died of myxomatosis. …
The Chateau Maillebois is a striking
turreted medieval house lying in a beautiful
wooded estate of 600 acres with a farm and
small river, the whole enclosed with a high
stone wall. This wall is broken only by
certain entrance gates which had been
rendered rabbit-proof before the introduction
of the virus. Thousands of wild rabbits were
devouring the farm crops and killing the
tender forest trees, Dr Delille’s son told us,
when in June, 1952, two wild-caught rabbits
were inoculated with myxoma virus. In six
weeks about 98% of the wild rabbits were
dead, but none of the domestic rabbits in the
hutches on the estate was affected.
Fig. 9.1. Paul F. Armand Delille (1874–1963). Born
in Fourchambault (Nièvre) in 1874, Delille
graduated in medicine and became one of the
leading paediatricians in Paris, carrying out
distinguished research on tuberculosis and infectious
diseases of children. He was appointed a professor in
the Paris Medical School and served as vice-president
of the Société de Biologie. During the First World War
he was Chief of Bacteriology in l’Armée d’Orient and
carried out valuable work on malaria, for which he
was made a Commander of the Legion of Honour. He
retired to a 300 hectare walled estate at Maillebois,
outside Paris. His relevance to this book derives from
the fact that in 1952, at the age of 78, he introduced
myxomatosis to France and thence to Europe by
inoculating two rabbits on his estate with virus
derived from a type culture collection in Lausanne,
an act for which he was reviled by rabbit breeders,
furriers and hunters but praised by farmers and
foresters.
In October 1952, the disease was identified
from a corpse picked up near Rambuoillet,
the residence of the President of France, fifty
kilometres from Maillebois.
The disease at Rambouillet was identified
as myxomatosis by Jacotot and Vallée (1953),
but at the time its source was unknown to
the authorities or the public. Concerning the
escape from Maillebois, Delille did not
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believe that the virus had been carried by
mosquitoes, because his own domestic
rabbits had not been affected. He thought
that perhaps other landowners had broken
in and captured diseased rabbits for
distribution on their properties. About a
year later, by which time some 35% of
domestic rabbits and an estimated 45% of
wild rabbits in France had died of
myxomatosis, Delille made a public statement. On 14 June 1953 and again on 14
October 1953, he read papers to the
Académie d’Agriculture, claiming that the
method should be used systematically for
rabbit control (Delille, 1953). At this time,
one of us (F.F.) was in Paris, and could not
but be amused by the controversy then
raging in Le Temps about the height that a
rabbit could jump, because this had been
proposed as the way by which an infected
rabbit had escaped from Maillebois.
While agriculturalists and especially
foresters supported Delille, and were
ultimately to award him a gold medal (Fig.
9.2), he was vigorously denounced by the
powerful hunting organizations. The
Ministry of Agriculture was in a difficult
position, because in addition to its duties in
relation to agriculture and forestry, it was
responsible for the Conseil Supérieure de La
Chasse, which derived its income from gun
licence revenue paid by sportsmen who
were primarily interested in hunting rabbits.
Bills were introduced into the French
Assembly to make the introduction and use
of myxomatosis illegal, but it was too late –
Fig. 9.2. Medal presented to Dr P.F. Armand Delille
by French agriculturists and foresters, at a ceremony
organized by M. Chavet, Secrétaire général de la
Fédération nationale des Producteurs de Bois et
Reboiseurs francais.
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the disease was established and spreading.
With the financial support of the hunting
clubs of France, a test case was brought
against Delille by the owner of a local
domestic rabbitry, all of whose rabbits had
died of myxomatosis. The case failed on a
technicality – it could not be proved that
the virus had been introduced directly into
the affected rabbitry by Delille (as indeed it
had not).
The virus that Delille had used differed
from those used previously for introductions
into European rabbits, which were derived
from the Moses strain and had been extensively passaged in laboratory rabbits. It was
sent to Delille by his friend Professor
Hauduroy, Director of the Centre de
Collection de Types microbien in Lausanne,
Switzerland2. Dr G. Bouvier, Director of
Institut Galli-Valerio in Lausanne, has
described the origin of this strain (Bouvier,
1954), which was derived from the
Sylvilagus reservoir in Brazil with at most
six passages in domestic rabbits before being
sent to Delille. It has been called ‘Lausanne’
in scientific papers since a description of its
properties by Fenner and Marshall (1957).
Attitude to Rabbits in France
Myxomatosis was a subject of great public
interest in France, because there was a
large commercial rabbit-breeding industry,
many people had back-yard hutches
(‘clapiers’) and there was a large and influential hunting fraternity for whom the wild
rabbit was an important resource. On the
other hand, foresters and farmers were very
much aware of the importance of rabbits as
an agricultural pest (Fig. 9.3). They shared
with wild boars the distinction of being
regarded as the major vertebrate pest, and
in 1952, before the advent of myxomatosis,
rabbit damage to agriculture and forestry
had reached an estimated annual cost of
1000 million francs and 88 of the 90
départmentes in France had declared the
rabbit a pest (Siriez, 1957).
The French Game Act of 1844, with
later amendments, protects wild rabbits as
game; predators which attack rabbits or
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Fig. 9.3. The place of the rabbit (wild and domestic) in France as it was before myxomatosis. (From Fenner
and Ratcliffe, 1965; modified from Barthélémy, 1953.)
game birds, such as foxes, stoats and
weasels, are regarded as vermin. There is
an open season for hunting rabbits between
early September and early January, with
possible extension to 31 March. In 1952,
the year before the introduction of
myxomatosis, 1,850,000 shooting permits
were issued, of which some 80% were held
by persons who were primarily rabbit
hunters. The importance of adequate
numbers of wild rabbits to these enthusiastic chasseurs is obvious (see Table 9.1,
below), as well as their significance for the
supporting industries indicated in Fig. 9.3.
The major hunting organizations, the
Conseil Supérieur de la Chasse and the St
Hubert Club de France, made prolonged
and vigorous protests about the destruction
of rabbits by myxomatosis, and supported
such counter-measures as the vaccination
of wild rabbits with fibroma virus, the
introduction of cottontails from the United
States, and the introduction of resistant
rabbits from Australia, all to no avail.
Besides the importance of wild rabbits
for hunters, there was a large domestic
rabbit industry. In 1950 some 140 million
domestic rabbits were produced and
consumed annually in France, and many
retired workers were partly dependent
upon rabbit raising for their livelihood.
Because mosquitoes were major vectors
and myxomatosis was sweeping through
the wild rabbit population, many outbreaks
of the disease occurred among domestic
rabbits in the early 1950s.
Short books on myxomatosis soon
appeared (Radot and Lépine, 1953; ViratPilet, 1954) and a comprehensive twovolume monograph was published in
1972–73 (Joubert et al., 1972, 1973). The
spread of myxomatosis in France prompted
the organization of an International
Symposium on Myxomatosis by l’Office
Internationale des Epizooties in Paris in
November 1953, and there were special
sections on myxomatosis at the International
Veterinary Congress in Stockholm in August
1953 and at the International Congress of
Microbiology in Rome in September 1953.
Official Action on Myxomatosis
A Central Service for the Fight Against
Myxomatosis was set up by the Conseil
Superiéur de la Chasse on 16 July 1953,
responsible to Dr F. Barthélémy, Engineer in
Charge of Water and Forestry. It worked in
close collaboration with the Veterinary
Service, the Laboratory of Veterinary
Research and the Institut Pasteur. Details of
legislation providing for the control of
myxomatosis are set out in the monograph
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by Joubert et al. (1973). The French Rural
Code (RC) and Penal Code (PC) severely
penalize deliberate importation and spread
of infectious diseases of domestic and wild
animals (PC articles 452, 454–1, 31 October
1955). Some articles of the Rural Code
authorize the destruction of animal pests
(RC articles 393–395) and specify the
methods that can be used. Rabbits can be
shot, trapped or poisoned. Sanitary regulations of rabbit farms are strictly policed, and
farmers are required to maintain a register
containing all information on diseases of
their stock and vaccinations carried out.
No immediate official action was taken
when myxomatosis was first recognized in
October 1952. However, after the rapid
spread of the disease in Spring 1953,
decrees were published by the Ministry of
Agriculture on 27 May 1953 and 27 June
1953. These made myxomatosis a notifiable
disease and prohibited the movement of
rabbits in an infected area. Appropriate
measures were specified for the isolation
and disinfection of domestic rabbitries,
dead animals being incinerated and their
remains buried in quicklime. It was further
required that the sanitary status of rabbit
farms had to be published fortnightly in the
National Sanitary Bulletin (Ministerial
decree of 9 July 1953). Persons guilty of ‘the
voluntary propagation of an epizootic’ were
liable to imprisonment for a period of one
to five years. In the case of wild rabbits,
areas at risk had to be indicated by notices
bearing the words ‘Myxomatose, maladie
contagieuse du lapin’, and all rabbits within
the area were supposed to be destroyed.
However, strict as these regulations
seem to be, it was impossible to eliminate
the disease, and periodically outbreaks
continue to occur among wild rabbits, and
sometimes spread from them to domestic
rabbits which are not protected by vaccination or insect-proof screening.
Clinical Features of Myxomatosis as
Seen in France
Myxomatosis in France was initiated by the
inoculation of two wild rabbits with the
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Lausanne strain of myxoma virus; no further
inoculations of virulent virus were ever
made in the field. Laboratory studies in
Australia showed that the Lausanne strain
produced a disease (Fig. 9.4A) with more
protuberant lesions than those caused by the
Standard Laboratory Strain, initially used in
Australia for rabbit control. In experiments
conducted in Australia, challenge infections
of rabbits with increased innate resistance
showed that the Lausanne strain was also
Fig. 9.4. Clinical signs of myxomatosis caused by
strains of myxoma virus found in France during the
early stages of the epizootic in France. (A) Lesions
produced by the Lausanne strain. Rabbit
photographed 10 days after inoculation; it died on
the twelfth day. The primary lesion on the flank was
very large, protuberant and deep purple in colour.
The head was oedematous (‘leonine facies’) and the
eyes completely closed with a profuse conjunctival
discharge. The secondary lesions were also raised,
purple in colour and not demarcated from the
surrounding skin. (B) Lesions produced by the Loiret
55 strain. The photograph was taken on the 25th
day and the rabbit died next day. About one-third of
rabbits inoculated with this strain recovered. The
primary lesion was very large and exuded serum.
There were numerous secondary lesions all over the
body, the eyes were completely closed and the ears
hung down because of numerous lesions on the
pinnae. From Fenner and Marshall (1957), with
permission.
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more virulent than the Standard Laboratory
Strain, in that the case-fatality rate was
about 99% when the Standard Laboratory
Strain was associated with a case-fatality
rate of 60–80%3.
Attenuated strains of myxoma virus were
first recognized in 1955, in the département
of Loiret (Jacotot et al., 1955; Fig. 9.5). The
lesions produced by this strain (‘Loiret 55’)
retained the protuberance characteristic of
the Lausanne strain lesions (Fig. 9.4B) but
the disease evolved more slowly. In more
extensive tests the case-fatality rate was
65% and the mean survival time 33.1 days,
with a range of 19 days to recovery. It was
later designated as the prototype European
strain of Grade IV virulence.
Respiratory or non-myxomatous myxomatosis
In addition to the increase in the occurrence of attenuated strains characterized by
the usual protuberant skin lesions but
lower case-fatality rates (see below), in
1980 French scientists observed for the first
time a ‘respiratory or non-myxomatous’
form of the disease (Brun et al., 1981b;
Joubert et al., 1982). This syndrome was
characterized by a longer incubation period
(1–3 weeks), swelling of the eyelids accompanied by severe purulent conjunctivitis,
genital lesions, and prominent nasal
lesions accompanied by lacrimation and a
mucopurulent nasal discharge (Fig. 9.6; see
pp. 97 and 104). There were often pink or
red spots on the ears, but no nodular skin
lesions (Arthur and Louzis, 1988). Its
epidemiology is described below (p. 220).
Although initially described in domestic
rabbits raised by intensive husbandry and
vaccinated with the SG33 attenuated
myxoma virus vaccine (Chantal, 1981), this
syndrome was also seen among rabbits
kept under traditional husbandry and
sometimes in wild rabbits. It was often
accompanied by sterility and the abandonment of litters by farmed does.
The Spread of Myxomatosis in France
As commonly occurs when a dramatic
‘emerging’ disease breaks out, a number of
Fig. 9.5. Henri Jacotot (1896–1991). Born in Dijon
in 1896, Jacotot served in France in the 1914–1918
war and was decorated with the Military Cross.
Subsequently he graduated in veterinary science
and was posted to the Pasteur Institute at Nhatrang,
in Indo-China, in 1922, initially as chief assistant to
Alexandre Yersin. In 1927 he was appointed
Director of that institute. In 1948 he returned to the
Pasteur Institute in Paris as head of the service of
animal microbiology, a post which he occupied
until he retired in 1965 as a Professor Emeritus. In
Indo-China he studied the many veterinary and
zoonotic diseases found in that country and was
responsible for the construction of the building
currently used by the Pasteur Institute at Nharang.
After returning to Paris he took a leading role in the
investigations of myxomatosis in France, describing
the first recognized case in 1953, experimenting
with insect transmission and studying the changes
in virulence of the virus. A highly respected scientist
and recipient of many prizes, he was a member of
the Academies of Veterinary Science and of
Medicine and served as President of the former.
fantastic stories about its mode of spread
circulated during the early days of the
French epizootic (Lockley, 1953). The
consumption of grass that might have been
contaminated by myxomatous wild rabbits
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Fig. 9.6. Hutch rabbit showing signs of the
‘respiratory’ form of myxomatosis. Courtesy Dr A.
Brun.
was thought to transfer myxomatosis to
hutch rabbits, and motor cars which ran
over infected rabbits were blamed for
moving the disease to new districts. It was
commonly reported that there was a black
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market for myxomatous rabbits, up to 5000
francs being paid by landholders anxious
to get rid of a pest. However, it soon
became apparent that mosquitoes were
important vectors in France, and the
presence of such a highly mobile and
efficient vector provided an explanation for
the movement of the disease to new areas
(Fig. 9.7) and from wild to domestic
rabbits. In the early days of the outbreak,
there was often inadvertant transfer of
disease between rabbit farms via infected
rabbits still incubating the disease. Rabbit
fleas are as common amongst wild rabbits
in France as they are in Britain and
undoubtedly contribute greatly to maintenance of enzootic myxomatosis throughout the year.
Epidemiology
With the knowledge that mosquitoes had
been important vectors in Australia, it was
Fig. 9.7. The spread of myxomatosis in France between January and September, 1953. From Rogers et al.
(1994), after Joubert et al. (1972), with permission.
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soon shown that the prime suspect for transmission in the early epizootics in France4,
Anopheles maculipennis atroparvus, was an
effective vector (Jacotot et al., 1954).
Subsequently, quiescent rabbit fleas were
recovered from soil scrapings from deep
burrows that had been abandoned by rabbits
ten weeks earlier, following autumn
epizootics of myxomatosis, and myxoma
virus was recovered from these fleas
(Joubert et al., 1969). Arthur and Louzis
(1988) postulated that eventually an
enzootic–epizootic cycle involving reservoirs, vectors and susceptible rabbits
developed. They suggested that the virus
might overwinter in fleas in the soil of the
burrow, in rabbits convalescing from infection, and in hibernating mosquitoes that
might be contaminated with the virus. With
the onset of warm weather, sharp mosquitoborne epizootics occurred among wild
rabbits, rising to a peak in mid-summer and
extending into autumn. These spread into
domestic rabbits housed in non-mosquitoproof shelters.
Sightings of diseased rabbits fell when
the wild rabbit population became greatly
depleted in the mid-1950s, but after the
attenuation of the virus and growing innate
resistance in the rabbits in the late 1960s,
the numbers of rabbits increased again. The
seasonal and annual variations in
myxomatosis then seen resulted from the
interaction of the abundance of rabbits,
their immune status (which was influenced
by the age structure of the population) and
the abundance of vectors. The occurrence
of epizootics in southern France during
summer and autumn was due to the
concurrence of large numbers of aggressive
mosquitoes and the presence of nonimmune young rabbits. If there had been
no myxomatosis the previous year, outbreaks often occurred in the spring and
simulids and ceratopogonids were often
involved (Joubert and Monnet, 1975).
Spring outbreaks affected mainly young
rabbits that had not been infected the
previous summer, the resulting decrease in
breeding females greatly depressing reproduction. Infection is maintained by rabbit
fleas during autumn, winter and early
spring,
spread
then
being
slow.
Overwintering in the absence of obvious
disease may be due to the persistence of
virus on the mouth parts of fleas, which
can remain in a quiescent state for some
time in uninhabited burrows.
Impact on wild rabbits
Myxomatosis clearly had a major impact
on the number of wild rabbits that were
available for hunting, and the bag did not
reach even 20% of its pre-myxomatosis
level until the 1961–62 season, although
the recorded figures may partly reflect the
paucity of hunters as well as of rabbits
(Table 9.1). In the Sologne, a favoured
département for rabbit hunting, the mean
numbers shot per season (compared with
Table 9.1. Numbers of rabbits killed each hunting season in 25 hunts in France, before and after the
introduction of myxomatosisa.
1950–51
1951–52
1952–53
1953–54
1954–55
1955–56
1956–57
1957–58
1958–59
1959–60
1960–61
1961–62
aData
64,439,000
37,723,000
55,133,000
6,721,000
2,750,000
2,404,000
1,293,000
3,357,000
2,043,000
4,074,000
5,491,000
10,906,000
of which 80% were from two unaffected hunts
of which 87% were from one unaffected hunt
of which 50% were from one hunt
from Giban (1956) and personal communication to Fenner (1963).
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pre-myxomatosis figures) increased from
1.5% in 1953–58 to 13.5% in 1967–72 and
17.6% in 1972–77 (Arthur et al., 1980).
However, after rabbits began to build up in
numbers due to the presence of attenuated
strains of virus and greater innate
resistance, variations in the timing of major
outbreaks of myxomatosis in relation to the
hunting season caused large fluctuations in
the numbers of rabbits shot. National
surveys in France in 1977 and 1978
(Arthur et al., 1980) showed that rabbit
density varied from place to place depending on environmental factors, such as type
of soil and agricultural practice, and was
also affected by hunting pressure and
predation. At that time rabbits were most
abundant in north-western France and
much less common in the south and west,
where in contrast to pre-myxomatosis
times they often lived only in isolated
pockets. Twenty years later (1997) the
picture has not changed.
After the first disastrous epidemics, a
variety of measures were undertaken by
hunting organizations to mitigate the
impact of myxomatosis. Vaccination with
fibroma virus was carried out in an attempt
to preserve some rabbits for shooting and
hopefully to build up ‘barriers’ to the
movement of myxomatosis. Later it was
suggested that, as with domestic rabbits,
wild rabbits should first be injected with
fibroma virus followed 6–8 weeks later by
SG33, both being administered by jet injector (Joubert et al., 1982; Fig. 9.8). Other
early and unsuccessful methods for
preserving rabbits as game animals
included the introduction of cottontails
(Sylvilagus floridanus), both as game
animals and to hybridize with Oryctolagus,
and a proposal to import rabbits from
regions of Australia where innate
resistance was high.
Impact on domestic rabbits
Myxomatosis was spread by mosquitoes
from wild to domestic rabbits and initially
it devastated the rabbit-breeding industry;
it was estimated in 1954 that 30–40% of
the
industry
had
been
destroyed.
Vaccination afforded some protection, and
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Fig. 9.8. Louis Joubert (1922–1989). Born in
Grenoble in 1922, Joubert enrolled in the National
Veterinary School at Toulouse in 1939, graduating
with honours in 1945 and becoming assistant to the
Professor of Infectious Diseases. He continued his
studies in veterinary medicine and in pharmacy,
and in 1948 was appointed project director at the
Veterinary School in Lyon, where he advanced to
become a professor in 1962. His early research was
focused on the epidemiology of zoonotic diseases,
and after Jacotot had retired he became the leading
expert on myxomatosis in France, showing
particular interest in unusual insect vectors and
especially in the ‘respiratory’ or ‘amyxomatous’
form of the disease. He was the senior author of a
major book on myxomatosis, published in Paris in
1972–1973.
with the reduction of the size of the wild
rabbit reservoir of myxomatosis in the late
1950s new outbreaks in rabbitries became
less common. Initially fibroma vaccine was
used on a very large scale, amounting to
tens of millions of doses annually; later it
was used on a smaller scale, primarily to
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protect breeding animals. It was only
moderately effective, and after limited
trials with an attenuated myxoma virus
vaccine developed in California (Saito et
al., 1964), another attenuated vaccine
(SG33) was developed in France (Saurat et
al., 1978). Given to rabbits at 2–3 months
of age, it was effective for about a year after
vaccination. However, the use of the SG33
vaccine was found to have an immunosuppressive effect, which among rabbits
housed under conditions of poor hygiene
led to a variety of secondary bacterial
infections (Brun et al., 1981; Godard,
1980). In such circumstances it was recommended that fibroma virus should be used
for primary vaccination, followed by SG33
vaccine a month later.
The epidemiological cycle as seen in the
1980s differed according to the type of
husbandry (Arthur and Louzis, 1988). Under
conditions of traditional husbandry, in
animal quarters with open contact with the
outside world, the strains of virus were
usually of the traditional nodular type, and
were usually more lethal among the
(genetically) unselected domestic rabbits
than they were for wild rabbits. Outbreaks
usually occurred in the autumn; there was a
delay of 6–8 weeks between epizootic peaks
in wild and domestic rabbits, the domestic
rabbit peak coinciding with the arrival of
mosquitoes within farm buildings (Puech,
1980). This form of myxomatosis could be
prevented by efficient protection against the
entry of mosquitoes by netting, unless
animals harbouring the virus were brought
in during the purchase of breeding animals.
Respiratory or non-myxomatous myxomatosis
Under intensive husbandry within closed
mosquito-proof
buildings,
a
nonmyxomatous, pulmonary form of the
disease, in which respiratory signs
predominated, was most common (Brun et
al., 1981a; see p. 216). It appeared to be
transmitted by the inhalation of infective
particles, both experimentally (Chantal,
1981) and in the rabbit farms. The incubation period varied between one and three
weeks, and infection was manifested by
swelling of the eyelids, genital and nasal
lesions, lacrimation and a mucopurulent
nasal discharge. This occurred primarily in
premises in which there was poor ventilation and a high frequency of respiratory
disease, and episodes of this form of myxomatosis were likely to occur at any time of
the year. Most outbreaks occurred after
recent introductions of rabbits from farms
which had experienced infection during
the previous 2–3 months. Such animals
may have been incubating the disease for a
longer period than usual, or, it has been
suggested, they were asymptomatic carriers, in which reactivation occurred after
the stress of transfer to new premises.
Changes in the Virulence of the Virus
Attenuated strains of myxoma virus were
first recognized in 1955, in the département of Loiret (see Fig. 9.4B). Other strains
with a similar degree of attenuation were
soon found elsewhere in France (Fenner
and Marshall, 1955; Siriez, 1960); the
Table 9.2. The virulence of field strains of myxoma virus in France in 1953, 1962, and 1968, calculated on
the basis of mean survival times and expressed as percentagesa.
Virulence grade
Mean survival time (days)
Presumed case-fatality rate (%)
Year
1953b
1962
1968
aFrom
bFrom
I
9–13
>99
>99
11
2.0
Joubert et al. (1972), p. 132.
field observations.
II
14–16
95–99
IIIA
17–22
90–95
IIIB
23–28
70–90
IV
29–50
50–70
V
—
<50
19.3
4.1
34.6
14.4
20.8
20.7
13.5
58.8
0.8
4.3
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Myxomatosis in France
virulence of these strains was not altered
by several serial passages in the rabbit
testis (Jacotot et al., 1956). Of ten French
strains recovered in 1960–63, three were
classified as of Grade IIIA virulence, three
of Grade IIIB, three of Grade IV and one of
grade V (Fenner and Ratcliffe, 1965). More
221
recent data (Table 9.2) suggested that 15
years after the introduction of the virus a
few highly virulent strains were still
circulating, although the majority of strains
were moderately or highly attenuated.
Endnotes
1Basser Library Archives, MS143/25/5A. Letters; G. Remaudière to F.N. Ratcliffe (22 January 1952),
F. Fenner to Remaudière (15 February 1952) and reply (19 February 1952).
2Basser Library Archives, MS143/25/5A. Correspondence between G. Bouvier and Fenner about origins of ‘Lausanne’ strain, used to introduce myxomatosis into Europe.
3G.W. Douglas, personal communication to Fenner (1978), J.W. Edmonds and R.C.H. Shepherd, personal communication to Fenner (1982), published in Fenner, F. (1983). The Florey Lecture, 1983.
Proceedings of the Royal Society B218, p. 268.
4In a communication to Jacotot et al. (1954), M.E. Roubaud, an entomologist with special knowledge
of mosquitoes, commented: ‘Au point de vue de la transmission de la myxomatose dans le milieu des
clapiers, c’est cet anophèle A. maculipennis s. lat. qui apparait sans nul doute, en Europe, comme
devant jouer le rôle principal. Dans les bois, dans les garennes, parmi les lapins sauvage, ce sont
d’autres espèces culicidiennes qu’il convient d’incriminer, parmi lesquelles de nombreux Aedes,
l’Anopheles claviger (bifurcatus) et surtout l’A. plumbeus’.
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