D12278.PDF

Rev. sci. tech. Off. int. Epiz., 2012, 31 (3), 907-918
Foot and mouth disease and similar virus
infections in camelids: a review
U. Wernery & J. Kinne
Central Veterinary Research Laboratory, P.O. Box 597, Dubai, United Arab Emirates
E-mail: [email protected]
Summary
Foot and mouth disease (FMD) remains the most important animal disease. The
FMD virus is highly contagious and occurs almost exclusively among clovenhoofed animals such as cattle, sheep, goats, Bactrian camels and swine. Old
World camels (OWCs) and New World camels (NWCs) inhabit FMD-endemic
countries in South America, North and East Africa, and the Middle and Far East.
Results of experimental infection of OWCs with the virus, and several clinical
observations from the field over a century, confirm that the two closely related
camel species of Bactrian and dromedary camels possess noticeably different
susceptibilities to FMD. It is now certain that Bactrian camels can contract the
disease. In contrast, dromedaries are not susceptible to FMD and do not transmit
infection, even when in close contact with susceptible animals. The
susceptibility of NWCs to the FMD virus has been demonstrated in the field and
in experimental infection trials. However, these animals are not very susceptible
and do not represent a serious risk in transmitting FMD to susceptible animal
species.
Keywords
Camelids – Epidemiology – Equine rhinitis A virus – Foot and mouth disease –
Picornavirus – Susceptibility.
Introduction
Foot and mouth disease (FMD) remains the most
important animal disease. It is most feared in countries
with a large and efficient livestock industry. The virus is
highly contagious, occurring almost exclusively among
cloven-hoofed animals such as cattle, sheep, goats,
Bactrian camels and swine. Both wild and domestic
animals are affected. The disease is mainly characterised by
vesicular lesions, but necrotising degeneration of the
myocardium in calves has also been observed. Infection in
humans has been described but is rare and not considered
a public health risk (3, 33).
Old World camels (OWCs) inhabit countries in North and
East Africa, and the Middle (dromedary) and Far East
(Bactrian camel), whereas New World camels (NWCs) live
in South America. Most of these areas are endemic for
FMD. In the past few years our knowledge of the
susceptibility of camelids to the FMD virus has increased
through observations in the field and especially through
experimental infections (12, 25, 50).
Aetiology and epidemiology
Foot and mouth disease is caused by an RNA aphthovirus
of the family Picornaviridae. At least seven immunologically
distinct serotypes and over 60 subtypes of the virus have
been identified. There is no cross-immunity between
strains (26).
The disease is enzootic in parts of Europe, Africa, the
Middle East, India, the Far East and South America
(Fig. 1). North America, Australia, New Zealand and many
countries in Western Europe are free of the disease and
have stringent regulations preventing the introduction of
the virus. Foot and mouth disease is of great interest to
908
Rev. sci. tech. Off. int. Epiz., 31 (3)
No information
Never reported
Not reported in the period
Infection / Infestation
Clinical disease
Current disease event
Present for other serotype
Disease limited to one or more zones
Fig. 1
Map of foot and mouth disease outbreaks in 2011 (58)
camel owners because the disease is enzootic in many
countries where camelids are indigenous. Saudi Arabia, for
example, with a camel population of 800,000, imports
approximately 6.5 million live animals every year (mainly
sheep and goats) from Africa, Asia and Australasia (16, 17,
54). Animals from Africa and Asia bring their own strains
of the virus, which spread within the nomadic herds of
Saudi Arabia and neighbouring countries (57). It is of great
importance to know whether camels play a role in
transmission of the virus.
The natural hosts are artiodactyles, including cattle, pigs,
sheep and goats, as well as many wild animals. Many
ungulate species may become carriers; that is, the virus
persists in the oesophageal-pharyngeal region for more
than 28 days after infection but the animal does not display
clinical signs. The African buffalo (Syncerus caffer), for
example, may harbour the virus in its pharynx for up to
two years without developing vesicular lesions. In contrast,
American elk (Cervus elaphus nelsoni) (35) most probably
do not become long-term carriers.
Most transmission of the virus is via aerosols, usually when
animals are in close contact with each other, although
under certain circumstances the disease may spread over
long distances (31). Study of the epidemiology of FMD has
been revolutionised by the use of molecular techniques
that enable individual strains of the virus to be
characterised. Using these methods, it has been possible to
trace the movement of individual strains of the virus from
one country to another (21).
Foot and mouth disease in New World camels
Several experimental studies on the susceptibility of NWCs
to the FMD virus have been performed in the Americas,
and all were carried out on the domesticated NWC species,
the llama (Lama glama) and the alpaca (Lama pacos). Some
field reports on the susceptibility of NWCs to FMD are also
available, as well as a few serological surveys. No
information is available on the epidemiology of FMD in the
wild NWC species, guanaco (Lama guanacoe) and vicuña
(Vicugna vicugna).
The susceptibility of NWCs to the FMD virus has been
demonstrated both in the field and in experimental
infections. In one field study, alpacas that showed minor
clinical disease were associated with an FMD outbreak in a
Puno (Peru) cattle population. However, serotype A24 of
the virus was isolated only from the diseased cattle (29). In
other field studies the susceptibility of NWCs to FMD has
not been confirmed. Thus, during the 1981 outbreak of
FMD at the Assam Zoo in India, where a large number of
909
Rev. sci. tech. Off. int. Epiz., 31 (3)
ungulates were kept, including members of the camel
family, neither llamas nor dromedaries became infected
(39). In Argentina, 460 oesophageal-pharyngeal fluid
samples collected using the probang cup were obtained
from llamas of different sexes and ages under natural
pasture conditions where FMD outbreaks had occurred in
cattle. No FMD virus was isolated from any of the llama
samples (4, 6).
Inoculation and transmission studies have been conducted
in three countries: in Peru (28), in the United States at the
Foreign Animal Disease Diagnostic Laboratory (27) and at
the Instituto Nacional de Tecnologia Agropecuaria near
Buenos Aires, Argentina (11). All the experiments showed
that NWCs can be infected with various serotypes and
through different routes. Llamas and alpacas reacted with
mild-to-severe clinical signs. Nevertheless, transmission of
the virus to llamas and other susceptible animals was
demonstrated in only two of the investigations, in a limited
number of animals (27, 28).
The ability of the FMD virus to infect susceptible llamas
exposed either directly or indirectly to affected livestock
was evaluated in a well-executed study using virus
serotypes A79, C3 and O1 (11). Six pigs were inoculated
with the three serotypes by different routes. Thirty llamas
were placed with the infected pigs and later interspersed
with an additional 30 llamas after the initial exposure.
Forty susceptible livestock animals (pigs, bovine calves,
goats and sheep) were then added to the overall group of
60 llamas to detect possible transmission of the virus from
the llamas. Only two of 30 llamas directly exposed to the
infected pigs developed (minor) lesions, seroconverted,
and yielded virus in blood or oesophageal-pharyngeal
fluid. A third llama from this group seroconverted but
showed no lesions and did not shed virus. None of the
control animals introduced to the 30 contact-exposed
llamas developed lesions or antibodies and all failed to
yield any FMD virus.
All experimental studies on FMD in NWCs have clearly
shown that it was not possible to isolate FMD virus from
either oesophageal-pharyngeal fluid or blood more than
14 days post exposure. This is of paramount importance.
Unlike cattle, which are known to carry the virus for more
than three years (21, 26), llamas do not become carriers
(6, 27). It should be noted that not all animals coming into
contact with the FMD virus become persistently infected
and that carriers are not necessarily contagious. Under
experimental conditions, around 50% of cattle become
carriers. Both the animal species and the virus strain
appear to be determinants in the development and
persistence of the carrier state. Transmission of the virus by
carriers other than African buffaloes (Syncerus caffer) and
cattle has never been convincingly demonstrated (43). Pigs
do not become carriers (7) and eventually eliminate the
virus (21).
Although experimental infections in NWCs using differing
routes and virus serotypes have resulted in detection of
antibodies in routine serological tests (11, 27, 28),
serological field investigations (4, 6, 20, 34, 37) in llamas
and alpacas in South America did not reveal any antibodies
to the FMD serotypes tested. All the studies were
conducted on farms where NWCs were intermingled with
cattle, sheep and goats, as well as with wild ungulates.
Outbreaks of FMD had occurred on some of the farms,
with buccal, lingual and labial lesions in cattle (6).
Foot and mouth disease in Bactrian camels
Many old publications from the former Soviet Union
described outbreaks of FMD in the genus Camelus, but
without differentiating between the Bactrian camel and the
dromedary camel. This created some uncertainty among
the scientific community until Larska et al. (25)
demonstrated in intensive infection trials that FMD can be
contracted only by Bactrian camels and not by
dromedaries.
In Kazakhstan and Russia, several researchers (23, 24, 40,
41, 44, 47) reported on clinical signs of FMD in camels
that were clearly Bactrian. Their investigations were
summarised by Skomorochov (41) and Bojko and Suljak
(5) in their veterinary books. One of the first reports of
FMD in Bactrian camels goes back to 1893 (47) and
describes two forms of the disease: lesions in the mouth
and lesions at the feet. Kovalevskij (23) described the
clinical picture of FMD in Bactrian camels as resembling
lesions observed in cattle, with primary aphthae at the
virus entrance site and severe lesions on the feet. Increased
body temperature, hypersalivation and general weakness
were also noted. Another Russian researcher, Krasovskij
(24), observed several outbreaks of FMD in Bactrian
camels between 1921 and 1927 and began infection trials
in the animals. In these experiments, material from a cow
was injected into the scarified lips of a Bactrian camel,
FMD material from a pig was injected into the interdigital
skin of another Bactrian, and lymph fluid from an FMD
cow was injected intravenously into a third Bactrian. Only
the Bactrian camel that received the intravenous infection
developed the disease. Krasovskij concluded that
spontaneous FMD in Bactrian camels is rare and artificial
infection succeeds only when high virus doses are given
intravenously. Krasovskij also described an FMD outbreak
at Moscow Zoo in 1958/1959 in which 55 ungulates were
involved, including moufflon, ibex, deer, reindeer, musk
deer, llamas and camels. During this outbreak llamas and
camels were not affected, whereas other ungulates suffered
severe losses. Bojko and Suljak (5) described another
outbreak in 1958, near Astrakhan. On one camel farm,
32 Bactrian camels developed severe clinical signs of FMD
and a further 31 showed only mild lesions. The camels
were off their feed, developed an increased body
910
Rev. sci. tech. Off. int. Epiz., 31 (3)
temperature, the soles of the feet detached, and some of the
skin sloughed off at the carpal and tarsal joints, and at the
chest and knee pads. A clear exudate was visible
underneath the necrotic skin. Another comprehensive
description of natural FMD infection in Bactrian camels in
‘Middle Asia’ was provided by Kobec (22):
– 1st day: weakness, recumbency, no rumination, off
feed, 40.2°C fever, hyperaemic lips and gingival along the
tooth row
– 2nd day: fever 40.5°C, inside lips and along the tooth
mucosa and tip of the tongue small aphthae with yellow
fluid visible, aphthae had the size of peas, off feed,
recumbent, putrid nasal discharge
– 3rd day: 39.4°C, some aphthae had ruptured and
ulcers were visible, salivation with sticky threads
– 4th day: 37°C, ulcers start to heal, camel starts to eat
and ruminate, after six days camel was back to normal.
The author did not mention foot lesions but the camels
were recumbent.
Krasovskij (24) infected Bactrian camels artificially and
described the disease. After 48 h the first aphthae appeared
at the inoculation site, followed by blisters at the feet; all
the infected animals recovered after seven days. The
clinical signs of FMD in camels were described as similar
to those observed in cattle, but with less involvement of
the legs (5). Suckling camel calves that received milk from
affected dams developed viraemia followed by
gastroenteritis and death. Krasovskij also described
peracute cases with sudden death syndrome in Uzbekistan;
this probably resembles the known tiger heart disease in
bovine calves. The infection sources for FMD in camels are
sheep and goats, which are always kept together.
Regular outbreaks of FMD in East Asia continue to the
present day. The disease invaded the countries of East Asia
between 1997 and 2000, all outbreaks being caused by
FMD virus serotype O. In March 2000 the disease reached
Mongolia and eastern Russia (38). In Mongolia, the
subtype O/MNG/2000 infected cattle, sheep, goats and
Bactrian camels in which typical lesions were observed
(56). In May 2010 another serotype O outbreak in
Mongolia affected more than 25,000 livestock animals,
among which more than 20,000 were culled (50). Again
the Bactrian camel was also infected in this endemic, many
animals displaying typical lesions of FMD. One of the main
features was the detaching of the soles of the feet (Fig. 2).
This was the first time that an FMD virus had been isolated
from a Bactrian camel that showed typical clinical signs of
naturally acquired FMD.
The clinical signs that occurred during the FMD outbreak
in Mongolian Bactrian camels in 2000 were described by
Hohoo et al. (19) and appeared to resemble those observed
Fig. 2
Detachment of the soles of the feet resulting from natural
infection with foot and mouth disease virus in a Bactrian camel
(Courtesy of Dr D. Bold, Mongolia)
in cattle. However, it appears that no camel specimens
from these FMD outbreaks were sent to any investigation
centre; several isolates of the virus were dispatched to the
All-Russian Research Institute for Animal Health in
Vladimir but they all stemmed from cattle and none from
the camels. Moreover, although the World Reference
Laboratory for FMD at the Pirbright Institute in the United
Kingdom has received camelid samples for FMD diagnosis
at various times, including samples from the Middle East,
no FMD virus has ever been isolated from such samples.
Because of these uncertainties, scientists from the Central
Veterinary Research Laboratory (CVRL) in Dubai and from
Denmark conducted infection trials in both dromedary
and Bactrian camels (25). In a study in two Bactrian
camels, FMD virus serotype A from a suspension of bovine
vesicular epithelium was injected subepidermolingually
into the tongues of two animals (Fig. 3).
Fig. 3
Subepidermolingual injection of foot and mouth disease virus
serotype A into the tongue of a Bactrian camel
911
Rev. sci. tech. Off. int. Epiz., 31 (3)
Both camels developed moderate-to-severe clinical signs of
FMD with lameness of the hind feet, fever and recumbency
(Figs 4, 5 & 6), and both animals lost the entire soles of
both hind feet on day 14 post injection. The health of the
animals then gradually improved and the lesions healed
after 21 days. No lesions were observed at the inoculation
site on the tongue. Both camels developed high antibody
titres to the inoculated virus 7 to 10 days after injection.
Only low and transient amounts of virus were detected in
mouth swabs and probang samples. These findings
indicate that, although Bactrian camels become acutely
infected with FMD virus, they probably do not harbour the
virus in their pharynx for more than 14 days and do not
become long-term carriers.
Fig. 6
Severe lesions on the hind-leg footpads of a Bactrian camel
Du et al. (8) observed that, although there is no
information on receptors for FMD virus in camels,
integrins are likely to be important molecules in the
susceptibility of cloven-hoofed animals to FMD virus
infection. The close relationship of integrin genes from
Bactrian camels with those of pigs and cattle has been
demonstrated, and Du et al. (8) therefore postulate that
host tropism of FMD virus may in part be related to the
divergence in integrin subunits among different species.
Foot and mouth disease in dromedaries
Fig. 4
Lameness of the hind feet in a Bactrian camel, no lesions on the
front feet
Fig. 5
Recumbency and depression in Bactrian camels
Current knowledge on FMD in camelids was reviewed by
Wernery and Kaaden in 2004 (50). All observations on
natural and experimental FMD virus infection in
dromedaries have failed to show convincingly that this
camel species possesses the same susceptibility to the virus
as cattle and pigs. To date, there are only two field reports
where the FMD virus has been isolated from dromedaries,
and experimental research has been conducted in only
very few animals, with one serotype and in one country.
The results are published in little-known journals and the
design and executions of most of the experiments are
outdated. The conclusions are therefore questionable.
Scientists from Denmark and the CVRL in Dubai carried
out four infection trials with FMD virus serotypes O and A
in dromedaries in Dubai (2, 49, 52). High doses of virus
were inoculated subepidermolingually into a total of
23 camels (Fig. 7). The titre of the virus was
107.6 TCID50/ml as assayed in primary bovine thyroid
cells. Sheep and several other dromedaries were placed in
the same pen in direct contact with the inoculated animals.
Two heifers and two sheep inoculated with virus serotypes
O and A served as positive controls. Modern laboratory
techniques such as virus isolation, real-time polymerase
chain reaction (PCR), enzyme-linked immunosorbent
assay (ELISA) and virus neutralisation tests were used to
912
Rev. sci. tech. Off. int. Epiz., 31 (3)
surveys but not in others. In most of the investigations,
serum samples were taken from dromedaries that were
grazing together with cattle, sheep and goats and freeranging wild herbivores. No clinical evidence of FMD was
observed in the dromedaries, although many of them had
daily contact with infected ruminants (9, 18). Moreover,
many thousand dromedary sera in Africa and the United
Arab Emirates have been tested for evidence of FMD
antibodies but with negative results. Furthermore, no
antibodies were detected in testing samples from
1,119 dromedary milking camels with the Ceditest®
cELISA (53), which detects antibodies to field strains (nonstructural 3ABC proteins), and Habiela et al. (15) did not
detect any antibodies to FMD virus in 176 Sudanese
camels tested with a liquid-phase blocking ELISA.
Fig. 7
Subepidermolingual inoculation of a dromedary with foot and
mouth disease virus
Seroconversion has been reported in dromedaries in
Ethiopia and Egypt (1, 36). Nevertheless, Moussa (30) is of
the opinion that the antibodies identified by Richard (36)
were non-specific inhibitory substances frequently
observed in camel sera. The differences in serological FMD
results in dromedary sera noted by Abou-Zaid (1) can be
attributed to the laboratory methodology used. The ELISA
technique appears more sensitive than other tests for
detection of FMD antibodies. Several experimental
infections with FMD virus in dromedaries have revealed
that the animals do seroconvert. This was confirmed by
Frederiksen et al. (13), who vaccinated five dromedaries
against serotypes O, A and Asia 1 (triple vaccine Aftovax®).
Although the reaction of the camels to primary vaccination
was very limited, they reacted rather well to the second
vaccination. However, the serological response declined to
low levels 120 days after the second vaccination.
Fig. 8
Probang sampling of a dromedary
diagnose the infection. All inoculated and in-contact
animals were monitored and regularly sampled, including
with the probang cup (Fig. 8). None of the inoculated
dromedaries or contact animals showed any clinical signs
of FMD, whereas the positive control sheep and heifers
developed typical disease and seroconverted. None of the
inoculated dromedaries developed viraemia or specific
antibodies despite the high dose of virus inoculum. Unlike
Bactrian camels, dromedaries remain resistant to high
doses of FMD virus and therefore do not play any
significant role in transmitting the virus to susceptible
animals. There are similar differences between closely
related species of elephant: the African elephant (Loxodonta
africana) is resistant to FMD virus, whereas the Asian
elephant (Elephas maximus) is susceptible (46).
Several scientific papers deal with humoral antibody
production in dromedaries, both in field surveys and after
artificial infection. The results are contradictory, however:
virus antibodies were detected in some serological field
Diagnosis
The clinical signs of FMD are indistinguishable from other
vesicular diseases such as vesicular stomatitis, vesicular
exanthema of swine (calicivirus) and vesicular disease in
pigs (enterovirus of the Picornaviridae family). Laboratory
methods are therefore necessary for diagnosis (Table I).
There are several commercially available ELISAs that can
differentiate between field virus antibodies and vaccine
antibodies. The virus can be isolated on various cell lines,
including fetal camel kidney cells (10) and Vero cells (26).
Treatment and prevention
There is no cure for FMD. The most effective preventive
measure is to prohibit introduction of animals or animal
products into FMD-free countries from other countries
that have the disease. Many European countries have
banned routine vaccinations against FMD because most of
913
Rev. sci. tech. Off. int. Epiz., 31 (3)
Table I
Routine laboratory methods for diagnosis of foot and mouth
disease
Method
Materials
Technique
Virus isolation
Epithelial lesions
Primary calf thyroid cells
Vesicular fluid
IB-RS2 cells
Oropharynx material
(not preferred for virus
isolation)
BHK cells
Antigen detection
Epithelial lesions
CFT
Vesicular fluid
Immunocapture ELISA
Oropharynx material
RT-PCR (virus RNA)
neutralising antibodies to the picornavirus were found in
the fetal fluids and in two other llama herds with a similar
clinical syndrome of diabetes mellitus.
Equine rhinitis A virus was also isolated from aborted
dromedary fetuses during an abortion storm in Dubai (51).
Approximately 10% of the 258 breeding camels aborted at
six to eight months’ gestation. The dromedary herd had
direct contact with horses housed in a retirement home on
the outskirts of the camel camp. Among the 57 retired
horses tested, 80% were seropositive for the virus.
Although not proven, it was highly likely that the
dromedaries contracted their infection from these horses.
Blood (viraemic animals)
Serology
Serum
VNT
Liquid-phase blocking
ELISA, solid-phase
competition ELISA
Vaccinated animals:
3ABC ELISA
Immunoblot
BHK: baby hamster kidney cell line
CFT:
complement fixation test
ELISA: enzyme-linked immunosorbent assay
IB-RS2: porcine kidney cell line
RT-PCR: real-time polymerase chain reaction
VNT: virus neutralisation test
the outbreaks have been traced to improperly inactivated
vaccines or escape of the virus from the production site
(26). Furthermore, ruminants (cattle, in particular)
continue to carry live virus in their pharynx after contact.
Animals immune to FMD virus infection after vaccination
can still become carriers after contact with field strains
during outbreaks. Cattle can harbour the virus for up to
three years (21, 26). The vaccine against FMD is an
inactivated preparation; attempts to take advantage of new
molecular biological technology to produce better vaccines
have been unsuccessful. The duration of immunity after
FMD vaccination is rarely longer than six months (21). In
countries where vaccines are used, virus from an outbreak
must be typed to determine whether the field strain is
homologous to the current vaccine strain. There are no
official reports on FMD vaccines in camelids, although
experimental vaccination has been conducted in a few
dromedaries, achieving seroconversion (13).
Other picornavirus
infections in camelids
Equine rhinitis A virus infection in llamas was reported
(42) to have caused abortion in 15 animals over a threeand-a-half month period at an average gestation of
220 days. In addition to the picornavirus infection,
diabetes mellitus was also observed in the adult llamas.
The virus was isolated from two fetuses, and serum
Experimental infection of two pregnant dromedaries with
the isolated equine virus induced abortion in both animals,
thus fulfilling Koch’s postulates (51). The gross pathology
in all aborted fetuses retrieved from the field and in the two
aborted fetuses from experimentally infected dromedaries
was similar and revealed oedema of placenta and umbilical
cord. Severe subcutaneous, generalised oedema was
observed in all aborted fetuses and the abdominal and
thoracic cavities were completely filled with dark
haemolytic fluid. Diagnosis was based on serology (serum
neutralisation test) and virus isolation, on Vero cells, of
samples from placenta and fetal organs. Real-time PCR was
positive in this abortion outbreak.
It should be noted that placentation in Camelidae is diffuse
epitheliochorial, similar to that in equine species, and this
anatomical particularity may partly explain the
susceptibility of dromedaries to an equine virus. The
mingling of horses and camels should therefore be
avoided. There is no commercial vaccine for the protection
of camels from equine rhinitis A virus-induced abortion.
Another picornavirus, encephalomyocarditis virus, has
been isolated from a two-year-old dromedary in an
American zoological collection (48). Gross pathology
consisted of excessive pericardial fluid, epicardial
haemorrhages and pale foci within the myocardium. The
virus was isolated from the heart. It is believed that rodents
may have transmitted the virus.
Other vesicular diseases
resembling picornavirus
infections in camelids
Vesicular stomatitis (VS) is another vesicular disease,
indistinguishable from FMD, and is caused by a
rhabdovirus. There are two major types: New Jersey and
Indiana. There have been few studies on the susceptibility
of NWCs to VS virus. It is believed that natural infection
914
rarely occurs, as llamas that had been in close contact with
diseased cattle did not contract the disease (45). The
llamas even shared watering and feeding facilities with the
diseased cattle but did not seroconvert to VS virus. Further,
270 llamas serologically tested in Oregon were also
negative (32). Nevertheless, a natural case of VS in a single
NWC has been reported (12). Alpacas and llamas have
been shown to be susceptible to experimental infection
with VS virus. Vesicles appeared at the inoculation site at
the dorsum of the tongue and the animals developed fever
and anorexia (14). Fluids taken from the vesicles of the
NWCs caused disease in cattle. There are no reports on VS
in OWCs.
Conclusion
Research on FMD has been ongoing for many years,
reflecting the importance of this viral disease to trade and
livestock. Considerable progress has been made in
improving diagnostic tests and information exchange, and
collaborative networks have been established around the
world. The camelid family is now included in this progress
as a clearer picture of camelid susceptibility to FMD has
emerged from serious field investigations and experimental
trials.
The susceptibility of NWCs to FMD virus has been
demonstrated in the field and in experimental infection
trials. However, NWCs are not very susceptible and do not
harbour the virus in their pharyngeal mucosa for more
than 14 days. They therefore do not represent a serious risk
in transmission of the virus to susceptible animal species.
The results of experimental infections of Bactrian camels
with FMD virus, together with clinical observations from
the field over a century, confirm that the two closely related
camel species of Bactrian and dromedary camels possess
noticeably different susceptibilities to FMD. It is now
certain that Bactrian camels, in contrast to dromedaries,
can contract FMD.
Rev. sci. tech. Off. int. Epiz., 31 (3)
Diagnosis of FMD in Bactrian camels has been made not
only through clinical observations but also through
infection trials and by isolating the virus from field cases.
Under experimental conditions, these camels can be
relatively easily infected with the virus and develop the
disease. Future research into FMD in Bactrian camels
should now concentrate on field outbreaks. Samples from
suspected clinical cases should be sent to FMD reference
laboratories so that the epidemiology of FMD in Bactrian
camels can be better understood.
The lack of susceptibility of dromedary camels to FMD has
been shown in both field investigations and experimental
infection trials. These camels do not transmit infection,
even when in close contact with susceptible animals. The
World Organisation for Animal Health (OIE) Ad hoc Group
on Diseases of Camelids is expected to recommend that the
dromedary is removed from the list of FMD-susceptible
animals (55).
Acknowledgements
Many thanks go to the experts of the OIE Ad hoc Group on
Diseases of Camelids for their support: Dr Mehdi
el Harrak, Dr Bernard Faye, Prof. Mohammed Bengoumi,
Dr Abledmalik Khalafalla, Dr Daniel de Lamo and
Dr Tarun Kumar Gahlot.
The authors are very grateful to H.H. Sheikh Mohammed
bin Rashid al Maktoum and Dr Ali Redha for their longterm generous support.
915
Rev. sci. tech. Off. int. Epiz., 31 (3)
Le point sur la fièvre aphteuse
et d’autres maladies virales chez les camélidés
U. Wernery & J. Kinne
Résumé
La fièvre aphteuse demeure encore aujourd’hui la plus importante des maladies
animales. Le virus de la fièvre aphteuse, extrêmement contagieux, affecte
presque exclusivement les artiodactyles tels que les bovins, ovins, caprins et
porcins. Les camélidés de l’Ancien Monde (dromadaires et chameaux bactriens
en Afrique du Nord et de l’Est, au Moyen-Orient et en Extrême-Orient) et ceux du
Nouveau Monde (lamas et alpagas en Amérique du Sud) vivent dans des régions
où la fièvre aphteuse est endémique. Chez les camélidés de l’Ancien Monde, des
infections expérimentales ont confirmé les observations cliniques de terrain
depuis un siècle, à savoir que les chameaux bactriens et les dromadaires, qui
constituent deux espèces très proches, ne présentent pas la même sensibilité au
virus de la fièvre aphteuse. Il est désormais établi que les chameaux bactriens
peuvent contracter la maladie. En revanche, les dromadaires ne sont pas
sensibles à la fièvre aphteuse et ne transmettent pas l’infection, même lorsqu’ils
sont exposés à des animaux sensibles. La sensibilité des camélidés du Nouveau
Monde au virus de la fièvre aphteuse a été démontrée aussi bien sur le terrain
que lors d’infections expérimentales. Néanmoins, il s’agit d’une sensibilité de
faible intensité, de sorte que ces animaux ne présentent pas un risque élevé de
transmettre la fièvre aphteuse à d’autres espèces animales sensibles.
Mots-clés
Camélidés – Épidémiologie – Fièvre aphteuse – Picornavirus – Sensibilité – Virus de la
rhinite équine de type A.
Estudio de la fiebre aftosa e infecciones
víricas similares en los camélidos
U. Wernery & J. Kinne
Resumen
La fiebre aftosa es aún hoy la enfermedad animal de mayor importancia. El virus
que la provoca, extremadamente contagioso, afecta casi exclusivamente a
ungulados como bovinos, ovinos, caprinos y porcinos. Los camélidos del Viejo
Mundo y los del Nuevo Mundo viven en países donde esta patología es
endémica (en Sudamérica, el Norte y Este de África y el Medio y Lejano Oriente).
Los resultados de la infección experimental de camellos del Viejo Mundo con el
virus, así como varias observaciones clínicas realizadas sobre el terreno a lo
largo de un siglo, confirman que la susceptibilidad a la fiebre aftosa es
notablemente distinta en las dos especies de camélido estrechamente
emparentadas, el camello bactriano y el dromedario. Se sabe ahora con
seguridad que los camellos bactrianos pueden contraer la enfermedad. En
cambio, los dromedarios no son susceptibles a ella ni transmiten la infección,
aun cuando estén en estrecho contacto con animales susceptibles. En cuanto a
916
Rev. sci. tech. Off. int. Epiz., 31 (3)
los camélidos del Nuevo Mundo, mediante observaciones sobre el terreno y
ensayos de infección experimental se ha demostrado que son susceptibles al
virus. Sin embargo, ni el grado de susceptibilidad es muy elevado ni estos
animales entrañan un grave riesgo de transmisión de la fiebre aftosa a especies
susceptibles.
Palabras clave
Camélidos – Epidemiología – Fiebre aftosa – Picornavirus – Susceptibilidad – Virus A de
la rinitis equina.
References
1. Abou-Zaid A.A. (1991). – Studies on some diseases of camels.
PhD thesis. Faculty of Veterinary Medicine, Zagazig
University, Egypt.
2. Alexandersen S., Wernery U., Nagy P., Frederiksen T. &
Normann P. (2006). – Dromedaries (Camelus dromedarius) are
of very low susceptibility to experimental high dose
inoculation with FMDV serotype O and do not transmit the
infection to direct contact camels or sheep. In Report of the
Session of the Research Group of the Standing Technical
Committee of the European Commission for the Control of
Foot-and-Mouth Disease, 16–20 October, Paphos, Cyprus,
158–164.
3. Bauer K. (1997). – Foot-and-mouth disease as zoonosis. Arch.
Virol. Suppl., 13, 95–97.
4. Blanco Viera J., Marcovecchio F., Fondevilla N., Carrillo B.,
Schudel A., David M., Torres A. & Mebus Ch. (1995). –
Epidemiology study of foot-and-mouth disease in the llama
(Lama glama) in Argentina. Vet. Argent., 12 (119), 620–627.
5. Bojko A.A. & Suljak F.S. (1971). – Foot-and-mouth disease:
biological and ecological aspects of the problem [in Russian].
Kolos, Moscow, 117–161.
6. David M., Torres A., Mebus C., Carrillo B.J., Schudel A.,
Fondevilla N., Blanco Viera J. & Marcovecchio F.E. (1993). –
Further studies on foot-and-mouth virus in the llama. Proc.
Annu. Meet. U.S. anim. Hlth Assoc., 97, 280–285.
7. Donaldson A.I. (1987). – Foot-and-mouth disease: the
principal features. Irish vet. J., 41, 325–327.
8. Du J., Gao S., Chang H., Cong G., Lin T., Shao J., Liu Z.,
Liu X. & Cai X. (2009). – Bactrian camel (Camelus bactrianus)
integrins v 1 and v 6 as FMDV receptors: molecular cloning,
sequence analysis and comparison with other species. Vet.
Immunol. Immunopathol., 131 (3–4), 190–199.
9. Farag M.A., al-Sukayran A., Mazloum K.S. &
al-Bukomy A.M. (1998). – The susceptibility of camels to
natural infection with foot and mouth disease virus. Assiut vet.
med. J., 40 (79), 201–211.
10. Farid F., Tantawi H.H., Abd El Galil G.A., Saber M.S. &
Shalaby M.A. (1974). – Multiplication and titration of foot
and mouth disease virus in the foetal camel kidney tissue
culture. J. Egypt vet. med. Ass., 34 (3–4), 384–392.
11. Fondevila N.A., Marcovecchio F.J., Blanco Viera J.,
O’Donnell V.K., Carrillo B.J., Schudel A.A., David M.,
Torres A. & Mebus C.A. (1995). – Susceptibility of llamas
(Lama glama) to infection with foot-and-mouth-disease virus.
J. vet. Med. B, 42, 595–599.
12. Fowler M.E. (2010). – Foot-and-mouth disease. In Medicine
and surgery of camelids (M.E. Fowler, ed.), 3rd Ed.
Wiley-Blackwell, Ames, Iowa, 179–181.
13. Frederiksen T., Borch J., Christensen J., Tjørnehøj K.,
Wernery U. & Alexandersen S. (2006). – Comparison of
FMDV type O, A and Asia 1 antibody levels after vaccination
of cattle, sheep, dromedary camels and horses. In Report of
the Session of the Research Group of the Standing Technical
Committee of the European Commission for the Control of
Foot-and-Mouth Disease, 16–20 October, Paphos, Cyprus,
243–247.
14. Gomez D. (1964). – Tests on the sensitivity of camelids to
vesicular stomatitis. Anales Segunda Cong. Nac. Med. Vet. y
Zoot. (Lima), 403–406.
15. Habiela M., Alamin M.A.G., Raouf Y.A. & Ali Y.H. (2010). –
Epizootiological study of foot and mouth disease in the
Sudan: the situation after two decades. Vet. Arhiv, 80 (1),
11–26.
Rev. sci. tech. Off. int. Epiz., 31 (3)
16. Hafez S.M., Farag M.F. & Al-Sukayran A. (1993). –
Epizootiology of foot and mouth disease in Saudi Arabia: II.
Current status on dairy farms and control measures in
operation. Rev. sci. tech. Off. int. Epiz., 12 (3), 817–830.
917
30. Moussa A.A. (1988). – The role of camels in the epizootiology
of FMD (foot and mouth disease) in Egypt. In The camel:
development
research.
Proc.
Kuwait
seminar,
20–23 October 1986, Kuwait. Food and Agriculture
Organization, Rome, 162–173.
17. Hafez S.M., Farag M.A., Mazloum K.S. & al-Bokmy A.M.
(1994). – Serological survey of foot and mouth disease in
Saudi Arabia. Rev. sci. tech. Off. int. Epiz., 13 (3), 711–719.
31. Moutou F. & Durand B. (1994). – Modelling the spread of
foot-and-mouth disease virus. Vet. Res., 25, 279–285.
18. Hedger R.S., Barnett T.R. & Gray D.F. (1980). – Some virus
diseases of domestic animals in the Sultanate of Oman. Trop.
anim. Hlth Prod., 12, 107–114.
32. Picton R. (1993). – Serologic survey of llamas in Oregon for
antibodies to viral diseases of livestock (MS thesis). Oregon
State University, Corvallis.
19. Hohoo A., Zerendordsh S., Zerendagava S. & Zohmonbaatar H.
(2001). – About the clinical symptoms of FMD in Mongolia
[in Russian]. Mongolian vet. med. J., 37 (2).
33. Prempeh H., Smith R. & Müller B. (2001). – Foot and mouth
disease: the human consequences. BMJ, 322 (7286),
565–566.
20. Karesh W.B., Uhart M.M., Dierenfeld E.S., Braselton W.E.,
Torres A., House C., Puche H. & Cook R.A. (1998). – Health
evaluation of free-ranging guanaco (Lama guanicoe). J. Zoo
Wildl. Med., 29 (2), 134–141.
34. Puntel M., Fondevila N.A., Blanco Viera J., O’Donnell V.K.,
Marcovecchio J.F., Carrillo B.J. & Schudel A.A. (1999). –
Serological survey of viral antibodies in llamas (Lama glama)
in Argentina. Zentralbl. Veterinärmed., B, 46 (3), 157–161.
21. Kitching R.P. (1998). – A recent history of foot and mouth
disease. J. comp. Pathol., 118, 89–108.
35. Rhyan J., Deng M., Wang H., Ward G., Gidlewski T.,
McCollum M., Metwally S., McKenna T., Wainwright S.,
Ramirez A., Mebus C. & Salman M. (2008). – Foot-andmouth disease in North American bison (Bison bison) and elk
(Cervus elaphus nelsoni), susceptibility, intra- and interspecies
transmission, clinical signs, and lesions. J. Wildl. Dis.,
44 (2), 269–279.
22. Kobec A.I. (1936). – Cited from: Skomorokhov A.L. (1952).
– Foot-and-mouth disease [in Russian]. State Publishing
House of Agricultural Literature, Moscow, Leningrad, 123.
23. Kowaleskij M.J.M. (1912). – Le Chameau et ses maladies
d’après les observations d’auteurs russes. J. Méd. vét.
Zootechn., 15, 462–466.
24. Krasovskij V.V. (1929). – About the sensitivity of camels for
foot-and-mouth disease [in Russian]. J. mod. vet. Med., 24.
25. Larska M., Wernery U., Kinne J., Schuster R.K., Alexandersen G.
& Alexandersen S. (2008). – Differences in the susceptibility
of dromedary and Bactrian camels to foot-and-mouth disease
virus. Epidemiol. Infect., 137 (8), 549–554.
26. Leforban Y. & Sumption K. (2010). – Foot and mouth
disease. In Infectious and parasitic diseases of livestock, Vol. I
(P. Lefèvre, J. Blancou, R. Chermette & G. Uilenber, eds).
Lavoisier, Paris, 299–324.
27. Lubroth J., Yedloutschnig R.J., Culhane V.K. & Mikiciuk P.E.
(1990). – Foot-and-mouth disease virus in the llama
(Lama glama): diagnosis, transmission, and susceptibility.
J. vet. diagn. Invest., 2 (3), 197–203.
28. Mancini A. (1952). – Tests on susceptibility of South
American camelids to foot-and-mouth disease. (Ensayos
sobre la receptividad de los anguenidos a la fiebre aftosa.)
Bol. Inst. Nac. Antiaftosa (Lima), 1 (2), 127–145.
29. Moro M. (1971). – Ectima. In La alpaca: enfermadades
infecciosas y parasitarias. Boletín Divulgación. Instituto
Veterinario de Investigaciones Tropicales y de Altura,
Universidad Nacional San Marcos, Lima.
36. Richard D. (1979). – Study of the pathology of the dromedary
in Borana Awraja (Ethiopia). Dissertation Médecine
Vétérinaire. Université Paris 12, Creteil.
37. Rivera H., Madewell B.R. & Ameghino E. (1980). – Serologic
survey of viral antibodies in the Peruvian alpaca (Lama pacos).
Am. J. vet. Res., 48 (2), 189–191.
38. Sakamoto K. & Yoshida K. (2002). – Recent outbreaks of foot
and mouth disease in countries of East Asia. Rev. sci. tech. Off.
int. Epiz., 21 (3), 459–463.
39. Sarma G., Das S.K. & Dutta P.K. (1983). – Outbreak of footand-mouth disease in deer in the Assam state zoo. Vet. Rec.,
113 (18), 420–421.
40. Skomorochov A.L. (1952). – Foot-and-mouth disease
[in Russian]. State Publishing House of Agricultural
Literature, Moscow, Leningrad, 123.
41. Skomorochov A.L. (1963). – Foot-and-mouth disease
[in Russian]. In Animal virus diseases (M. Orlov, ed.).
Agricultural Literature and Journals, Moscow, 97–98.
42. Stehman S.M., Morris L.I., Weisensel L., Freeman W.,
Del Piero F., Zylich N. & Dubovi E.J. (1997). – Case report:
picornavirus infection associated with abortion and adult
onset diabetes mellitus in a herd of llamas. In Proc. American
Association of Veterinary Laboratory Diagnosticians Annual
Conference, 18–24 October, Louisville, Kentucky, 43.
918
Rev. sci. tech. Off. int. Epiz., 31 (3)
43. Sutmoller P. & Casas Olascoaga R. (2002). – Unapparent foot
and mouth disease infection (sub-clinical infections and
carriers): implications for control. Rev. sci. tech. Off. int. Epiz.,
21 (3), 519–529.
53. Wernery U., Thomas R., Syriac G., Raghavan R. & Kletzka S.
(2007). – Seroepidemiological studies for the detection of
antibodies against nine infectious diseases in dairy
dromedaries (Part 1). J. Camel Pract. Res., 14 (2), 85–90.
44. Terentieva S.M. (1975). – The breeding of animals
[in Russian]. Kolos Izdatel’stvo, Moskva, 208–209.
54. Woodbury E.L., Samuel A.R., Knowles N.J., Hafez S.M. &
Kitching R.P. (1994). – Analysis of mixed foot-and-mouth
disease virus infections in Saudi Arabia: prolonged circulation
of an exotic serotype. Epidemiol. Infect., 112 (1), 201–211.
45. Thedford T.R. & Johnson L.W. (1989). – Infectious diseases
of New-World camelids (NWC). Vet. Clin. N. Am. (Food Anim.
Pract.), 5 (1), 145–157.
46. Thomson G.R., Vosloo W. & Bastos A.D. (2003). – Foot and
mouth disease in wildlife. Virus Res., 91(1), 145–161.
47. Vedernikov V. (1893). – Disease of camels [in Russian].
Archive for Veterinary Science, I (4).
48. Wells S.K., Gulter A.E., Soike K.F. & Baskin G.B. (1989). –
Encephalomyocarditis virus: epizootic in a zoological
collection. J. Zoo Wildl. Med., 20 (3), 291–296.
49. Wernery U. (2010). – Dromedaries are resistant to foot-andmouth disease (FMD), Bactrians are not. A review. In Proc.
International Camel Symposium, 7–11 July, Garissa, Kenya, 3.
50. Wernery U. & Kaaden O.-R. (2004). – Foot-and-mouth
disease in camelids: A review. Vet. J., 168 (2), 134–142.
51. Wernery U., Knowles N.J., Hamblin Ch., Wernery R.,
Joseph S., Kinne J. & Nagy P. (2008). – Abortions in
dromedaries (Camelus dromedarius) caused by equine rhinitis
A virus. J. gen. Virol., 89, 660–666.
52. Wernery U., Nagy P., Amaral-Doel C.M., Zhang Z. &
Alexandersen S. (2006). – Lack of susceptibility of the
dromedary camel (Camelus dromedarius) to foot-and-mouth
disease virus serotype O. Vet. Rec., 158, 201–203.
55. World Organisation for Animal Health (OIE) (2010). –
Report of the 2nd meeting of the OIE Ad Hoc Group on
Diseases of Camelids, 3-5 May, Paris, France.
56. World Organisation for Animal Health (OIE) (2010). – Event
summary: foot and mouth disease, Mongolia. Available from
the OIE World Animal Health Information Database:
www.oie.int/wahis_2/public/wahid.php/Reviewreport/Revie
w/viewsummary (accessed on 13 November 2010).
57. World Organisation for Animal Health (OIE) (2010). –
Situation of foot and mouth disease (FMD) in the Middle
East, June 2010. Available at: www.rr-middleeast.
oie.int/download/pdf/FMD-situation%20ME-2010_[1].pdf
(accessed on 13 November 2010).
58. World Organisation for Animal Health (OIE) (2011). –
Disease distribution maps: foot and mouth disease. Available
at: web.oie.int/wahis/public.php?page=disease_status_map&
disease_type=Terrestrial&disease_id=1&empty=999999&sta
_method=semesterly&selected_start_year=2011&selected_
report_period=1&selected_start_month=1&page=
disease_status_map (accessed in March 2011).