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Introduction
On 26 August 2004, the CNNR (National Reference Centre for Rabies - Pasteur
Institute) reported a case of rabies in a 4-month old puppy illegally
imported from Morocco to Bordeaux in France to the French public health
institute, the Institut de Veille Sanitaire (InVS). The animal, which
was neither officially registered nor vaccinated, was acquired in the
Moroccan region of Agadir and brought to France by car, via Spain,
on 11 July 2004. After becoming aggressive on 17 August , the dog's
condition rapidly deteriorated and it died on 21 August.
Rabies is a zoonosis caused by a rhabdovirus of the genus Lyssavirus.
The disease can be transmitted to humans via biting, scratching, or licking
of excoriated skin or mucosa; the incubation period typically ranges
from 1 to 3 months. If untreated during this phase, rabies infection
leads to fatal encephalomyelitis. France has been free of rabies in terrestrial
mammals since 2001. Fox rabies, which was first recorded in France in
1968, was eliminated following an oral vaccination programme for foxes
combined with increased control of stray animals [1].
An investigation was initiated by the DDASS (Departmental Health and
Social Services Division) and the DDSV (Departmental Veterinary Services
Division) of the relevant French districts and the CIRE (Inter-Regional
Epidemiology Centre-) of the Aquitaine region, in conjunction with the
health and food industry authorities, the CNNR and the InVS. The purpose
of the investigation was to identify all humans who had been in contact
with the puppy during the communicable risk period and to refer them
to a CAR (anti-rabies centre), the only structures in France empowered
to diagnose rabies and administer the post-exposure vaccination. The
investigation also aimed to locate all animals that had been exposed
to the virus ,in order to prevent rabies from being reintroduced in France.
The salivary excretion phase starts, at the earliest, 15 days before
the appearance of clinical signs and lasts until death. The puppy could
therefore potentially have transmitted the virus at any time between
2 and 21 August. During this period, the animal and its owner had travelled
to various locations in Gironde, Dordogne and Lot-et-Garonne, and spent
much time attending arts festivals. These events attract thousands of
visitors from France and other European countries (Figure 1). The puppy
was not constantly kept on a lead.
Methods
Because of the great number of humans and animals possibly in contact
with the puppy during the communicable risk period, the Gironde Prefect
set up a crisis centre in Bordeaux from 27 August to 22 September 2004.
An inter-ministerial crisis centre was also set up at the national
level. These centres expedited contacts between stakeholders, helping
to coordinate investigations and action plans. The centres included
all parties involved at the local and the national levels.
Investigation of contacts
The owner of the puppy was questioned and his trip to Aquitaine was retraced
in order to establish a list of potentially exposed humans and animals
during his travels between 2-21 August 2004.
An extensive media campaign was launched in order to encourage anyone
who had had contact with the puppy to get in touch with a ‘Centre
15’ (medical emergency service hotline) or the health authorities;
and to encourage owners of pets that had come into contact with the puppy
to consult a veterinarian or the local DDSV (veterinary organisation).
Pictures of the puppy and the description of the possible contacts based
on indications provided by the owner were regularly broadcast by the
media. Posters were sent to all of the DDASS for display in public places,
emergency services, Centre 15s, and the CAR.
An alert was sent to European Union (EU) member states' health authorities
via the HSSDC-EWRS network, and to third countries via the World Health
Organization (WHO) , to find potential contacts among citizens of other
countries. The dog's description and the places visited by the dog and
owner were issued. Additional information was sent to any country that
requested it, and the 'decision model form' used in France to define
'contacts presenting a risk' was sent to the European Commission's Directorate-General
of Health and Consumer Protection (DG-SANCO) and to the national health
authorities that requested it [2].The European health authorities and
the WHO were duly notified in order to locate possible contacts living
abroad [2].
A 24 hour hotline was set up in the Gironde prefecture every days until
22 September 2004, and the service then operated daily between 0800 and
1800until 15 October 2004. Based on the initial assessment lists, individuals
for whom contact was either ascertained or suspected (through biting,
scratching, or licking of excoriated skin or mucosa) with any puppy that
matched the description of the rabid puppy, or was compatible in time
and place) were directed to a CAR. After 8 September 2004 this procedure
was extended to include contacts with any carnivore that had come into
contact with the puppy and then disappeared, since these animals could
possibly be vectors.
Police handled questioning of witnesses and investigations to locate
possibly infected humans or animals.
A national hotline was made available between 10-22 September 2004.
All medical emergency services in France reported any cases of dog bites
in the Aquitaine region in August 2004 to the InVS. the CIRE and the
InVS then contacted the people who had been bitten to determine whether
the rabid puppy was involved.
Management of contacts
At the CAR, a risk assessment was made of all humans referred, to ascertain
whether post-exposure treatment was appropriate and, if so, to determine
what treatment should be prescribed (vaccine with or without rabies
immunoglobulin (RIG)) in accordance with WHO recommendations [3].
The DDSV and veterinary authorities identified animals that had been
in contact with the carrier.
Samples were analysed by the CNRR in cases of possible human exposure
and by the LNR (National Reference Laboratory for animal rabies) in cases
of possible animal exposure.
Results
Investigation of possibly infected subjects
In addition to the seven humans and two dogs within the immediate environment
of the puppy, a search was initiated to locate and additional 13 people
and 17 dogs, based on information provided by the owner and additional
accounts by witnesses. Of these, eight people and five dogs were found.
The hotline in the Gironde prefecture received 3500 calls in 50 days;
the DDASS and the DDSV in the Dordogne and Lot-et-Garonne regions received
29 and 61 calls respectively, and the national hotline received 483 calls.
In all, 429 people were advised to contact a CAR. Of the people referred
, 40% had no connection with the rabid animal. One hundred and sixty
two calls were followed up with a veterinary investigation.
Feedback from emergency wards yielded only one person, which had already
been identified by a crisis centre.
Post-exposure treatments
Post-exposure treatment for rabies was prescribed to 187 subjects, 147
(79%) of which were treated in the Bordeaux CAR. Fifty four per cent
of subjects were male (the male to female ratio was 1.15). The mean
age, as derived from data available on 176 subjects, was 17 years.
Ages ranged between 1 and 83 years with a median of 9 years.
The puppy was clearly identified by 29 of the treated subjects (16%).
In four cases, an animal had been in contact with the puppy during the
exposure risk period. Half of those treated had attended the Festival
de Libourne (TABLE 1). The type of contact was undetermined in 58 cases,
especially for young children (TABLE 2). In total, 8 people were bitten,
5 by the identified animal.


A four-injection course of treatment was used for 94% of cases. One person
was treated by a series of five injections followed by injection of
immunoglobulin. In total, eight people were treated by serovaccination.
Veterinary laboratory
Over a period of six months more than 1200 animals, the majority of which
had been found dead, were analysed in the three relevant departments
in the Aquitaine region of France.
A total of 57 animals that were confirmed as having had contact with
the puppy (including six from outside the Aquitaine region) were identified
and analysed.
Testing found no evidence of rabies virus.
In addition, 759 stray animals that had been impounded by authorities,
and that could not be identified as having escaped from their owners,
or that had no evidence of having had a rabies vaccine, were monitored
for a period of one year, in compliance with applicable legislation in
the region.
Discussion
The last case of human rabies contracted in France was reported in 1924;
cases of imported human rabies are rare with only 20 cases recorded
between 1970 and 2003 [4]. At present, rabies in France is considered
to be a traveller’s disease, as it is in many other European
countries [5]. A few human cases are regularly reported in EU rabies-free
countries [6]
However, there is a risk of contracting the disease in France due to
illegal importation of animals from enzootic rabies areas [7,8]. Two
other cases of rabies were diagnosed in Lorient and Bordeaux in 2004,
in dogs that had been illegally brought to France from Morocco, via Spain.
These two cases led to the vaccination of 24 and 11 people, respectively
[9,10]. A total of 22 cases of imported canine rabies have been reported
in France since 1968.
In the case described here, the level of risk was thought to be significant
because of the large number of humans (attendance at the festivals was
estimated at 80 000) and animals potentially exposed, and due to extensive
geographical scattering.
Identification of contacts at risk, in order to insure that they received
appropriate care, relied on the timely transmission of information, because
of the large number of non-French citizens present at the locations visited
by the dog. The management of this crisis at the international level
highlights the essential role of a European level rapid alert system
and the need for complete transparency in the case of a threat involving
member states.
At the national level, the situation was managed through close cooperation
between the various organisations involved, which made it possible for
a large number of potentially infected humans to be treated. Furthermore,
as a consequence of this episode, a substantial increase in activity
at the CAR was noted due to increased awareness regarding the risk of
rabies on the part of the medical community and the general public.
In parallel with efforts to locate exposed humans and animals, control
measures concerning the circulation of the domestic carnivores and stray
animals were reinforced locally in the Aquitaine region for a period
of six months [11-12].
Six months after the death of the rabid animal, none of the subjects
treated showed any signs of rabies infection and no cases of secondary
animal rabies had been declared.
The five people who were sought but not found had been described by eyewitness
testimonies, and we cannot be sure either of that these people were exposed,
or that they were described accurately.
The recurrence of this type of alert, underlines the necessity to control
the importation of domesticated and wild animals. Health inspection regulations
for animals brought into the European Union must be strictly applied
[13]. Importers of domesticated carnivores originating in countries where
rabies has not been eradicated must provide animal identification and
proof of vaccination; animals must also test positive for rabies antibodies.
Travellers to rabies enzootic areas should been informed of the risk
to public and animal health that illegal importation of animals can engender.
The list of the countries at risk must be made widely available to physicians
and the public.
Acknowledgements
We wish to thank everyone and all the organisations that have contributed
to this investigation : the French anti-rabies centres; the French Centres
15; the crisis centre of the Gironde prefecture composed of staff from
the Departmental Health and Social Services Division (DDASS) and the
Departmental Veterinary Services Division (DDSV) from the Gironde department,
the veterinary services of the Army, the DRASS, the CIRE Aquitaine as
well as the Police and Constabulary departments; the DDASS and DDSV from
Dordogne and Lot et Garonne departments; the departmental veterinary
laboratories of Gironde, Dordogne and Lot et Garonne departments; the
liberal and hospital practitioners and the surveillance network of the
French veterinary services; the Regional Union of liberal practitioners
of the Aquitaine department. Teams of National Reference Laboratory for
animal rabies and National Reference Centre for Rabies
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