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Despite measures taken in France since 1990 to
control the spread of bovine spongiform encephalopathy (BSE), the
incidence of BSE cases notified in France by the BSE Epidemiological
Surveillance Network has been rising in recent years. By 1 July 2000, 103
cases of BSE had been detected, including 74 ‘born after the ban’
(BAB) cases. This increase expresses the changes over time in both the
real incidence of the disease and in disease surveillance.
In 1988, the role of meat and bone meal (MBM) in the transmission of
bovine spongiform encephalopathy (BSE) was shown (1). These animal
foodstuffs are prepared with animal by-products from the slaugtherhouse
and rendering plants. Changes to the rendering process (lowering of the
temperature and change of the fat extraction process) of MBM led to a
failure of an infectious agent inactivation and had been therefore
associated with BSE. The European Union (EU) had become aware of the risk
that the British epidemic might spread to other European countries as a
result of British exports of MBM and decided to add BSE to the list of
notifiable diseases (Decision 90/134/EEC). It then made it a requirement
for member states to investigate clinical cases of BSE (Decision
90/200/EEC). Under French law, this resulted in the setting up of a BSE
epidemiological surveillance network, which became operational at the end
of 1990 (2). The network detected the first case of BSE in France on 28
February 1991. In August 1989, French regulations were introduced that
prohibited imports of MBM from the United Kingdom as cattle feed and, in
July 1990, the use of mammalian meal in cattle feeds. Despite those
measures to prevent the disease from spreading, cattle were contaminated
– as of May 1996, the first ‘born after the ban’ (BAB) cases were
detected. Taking into account the time taken to deplete feed stocks, those
animals were born after 1 January 1991. This article reviews the frequency
of BAB cases in France to date and the hypotheses concerning the origin of
these cases.
BSE surveillance and control – case investigations
The BSE epidemiological surveillance network is based on the systematic
surveillance of cattle aged over 2 years presenting with neurological
disorders, by using a defined list of criteria (age, symptoms, course of
disease) (3)). In addition, BSE surveillance has been extended to all
animals notified with suspected rabies in the context of the national
surveillance scheme for rabies. Clinical suspicions are raised either on
farms, by veterinary practitioners , or in slaughterhouses, by
veterinarian inspectors, and then confirmed by a county coordinating
veterinarian specially trained for that purpose. After slaughter, the
diagnosis is confirmed by the reference laboratory of the French Agency
for the Food Sanitary Safety (Agence Française de Sécurité Sanitaire
des Aliments, AFSSA) in Lyon by histology, or Western blot,when the sample
is of poor quality. Subsequently, and particularly in May 1999,
surveillance was intensified by introducing in depth control of animals
subjected to emergency slaughtering and imported animals born in Portugal
or Switzerland, and, in November 1999, by control of a quota of
certain culled animals, i.e. animals too old to be used for breeding
purposes and sent to be slaughtered (2).
Since 1996, the National Brigade for Veterinary and Health Inquiries
(Brigade Nationale d'Enquêtes Vétérinaires et Sanitaires, BNEVS) has
conducted an in depth epidemiological investigation in each farm affected
by BSE (4). The investigation is based on an interview with the farmer and
an analysis of the farm's registers and accounts, and addresses the status
of the infected animal’s mother, its diet since birth, the suppliers of
the commercially available feeds distributed, the presence of other animal
husbandry units on the farm, the use of organic fertilisers from outside
the farm, and medications used. Further investigations are carried out on
the premises of the cattle feed manufacturers supplying the farm, to
evaluate the potential contamination of the feeds by products of rendering
plants.
Control of the spread of BSE has become stricter over time. The
prohibition of mammalian meals for cattle feeds was extended to feeds for
all ruminants (July 1994) and, since July 1996, has covered all proteins
of animal origin (with the exception of milk protein). In addition, beef
offal associated with a specified risk and carcasses from dead animals
were prohibited in the manufacture of animal meals in April and June 1996,
respectively. Lastly, heat treatment of MBM, in compliance with
recommendations by the European Community (133°C, 3 bars, 20 min)
became mandatory in February 1998 (2).
Epidemiological data on 1 July 2000
By 1 July 2000, 103 cases of BSE had been detected in France (figure
1), 74 (72%) of which were BAB cases. Since 1997, almost all of the cases
observed have been BAB cases (figure 2) The number of cases detected per
year has been rising since 1997 and reached 31 in 1999. This means an
annual incidence of 2.7 per million cattle aged over 2 years (5). Most of
the BAB cases were born during the second half of 1993 and in 1994 (figure
3).


The investigations conducted by BNEVS have yielded information about
the BAB cases. Vertical transmission from mother to offspring seems to be
excluded in most cases since the infected animal’s mother was still
alive more than one year after its birth in 85% of the cases emerging in
1999. In contrast, at the current stage of the inquiries, in no case can
all risk of feed related contamination be excluded with certainty.
Complementary feeds that are not produced on the farm, made from various
ingredients, and given additionally to foodstuffs produced in the farm,
are commonly used, at least during the first year of an animal's life. In
all cases, the plausibility that a feed probably consumed by the animal
had been cross contaminated by products likely to be entirely or partly
derived from high risk ruminant byproducts has been demonstrated.
Contamination may have occurred during feed manufacture, transport, or
distribution.
Discussion and conclusion
The increased incidence of BSE cases in recent years is to be
interpreted as a function of two variables whose effects are linked:
firstly, the changes over time in the real incidence of the disease and,
secondly, the changes over time of disease surveillance. Surveillance has
become increasingly effective over time, which has led to a rise in the
number of clinically suspected cases each year and hence an increase in
the additional controls imposed on emergency slaughtering and culled
animals. As a result, it is impossible to estimate the rise in the real
incidence of BSE: the rise in the observed incidence may in part be
related to an increase in the effectiveness of surveillance.
Retrospective case studies argue in favour of one of the hypotheses
concerning the sources of contamination of BAB cattle formulated by the
French expert committee on transmissible subacute spongiform
encephalopathies (TSSEs) and prions in the committee's opinions dated 17
December 1998 and 27 February 1999 (6) – namely, a dietary source
related to cross contamination between feeds for non-ruminants and feeds
for ruminants. In 1993 and 1994, when most of the cases were born, the
animal tissues associated with the highest risk (the brain and spinal
cord) and the carcasses from dead animals were not excluded from MBM
manufacture. During those years, animal meal was potentially contaminated
by tissues from French cattle dying at the end of their incubation period,
or for which the disease was not detected, and in addition MBM was
imported from various EU countries. Besides, a high tonnage of cattle
carcasses was imported from the United Kingdom. This may also have caused
contamination of animal meals used in products for non-ruminants. The
hypotheses on the origin of the BAB cases could be investigated by means
of the case control study of farmers' practices with regard to cattle
feeds and supply sources, whose project was validated by the French expert
committee.
Given the stringent measures taken since 1996 to improve control of BSE
and the four to five year interval required to observe the effects of
those measures (mean incubation period), a marked decrease in the real
incidence of BSE is expected as of 2002. The decrease could be masked by a
qualitative change in BSE surveillance, with the introduction of a
screening programme in July 2000 for cattle that die or are humanely
slaughtered on farms, and cattle subject to emergency slaughter after an
accident.
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