Download 40. FMD and camelids

Appendix 40
FMD and camelids: International relevance of current research
U. Wernery
Central Veterinary Research Laboratory, P.O. Box 597, Dubai, U.A.E.
Key words: Tylopoda, camelids, FMD
Abstract
Camelids regurgitate and re-chew their food and thus technically ruminate. In strict taxonomic terms,
however, they are not recognized as belonging to the suborder Ruminantia. They belong to the suborder
Tylopoda. Numerous differences in anatomy and physiology justify a separate classification of tylopods
from ruminants. Many reports show that New World Camelids (NWC) and Old World Camelids (OWC)
possess a low susceptibility to foot and mouth disease (FMD), and do not appear to be long-term carriers
of the foot and mouth disease virus (FMDV). Recent preliminary results from Dubai have shown that two
dromedaries infected subepidermolingually with FMD serotype 0 did not develop any clinical signs and
failed to develop any lesions at the inoculation site. Infectious FMDV or FMDV RNA were not isolated and
the two dromedaries failed to seroconvert.
It would, therefore, appear appropriate for OIE to refine the definition of NWC and OWC by clearly stating
that these animal species are not members of the suborder Ruminantia. Furthermore, these recent
results suggest that dromedaries (and most probably all camelid species), which are listed in the OIE
Code chapter as being susceptible to FMD similar to cattle, sheep, goats and pigs, are much less
susceptible or non-susceptible to FMD. Therefore, the importance of FMD in camelids should be reassessed. The Central Veterinary Research Laboratory (CVRL) in Dubai, U.A.E., offers to become a
reference laboratory for OWC. For more than a decade, CVRL has published in excess of 150 scientific
papers and three reference books on camel diseases.
Classification, population and distribution
Although camelids ruminate, they are not modified ruminants in a taxonomic sense. A separate
evolutionary history of 35 – 40 million years divides tylopods from ruminants. Camelidae belong to the
suborder Tylopoda (Fowler, 1997; Table 1). Numerous anatomical and physiological differences justify
the separate classification of Tylopoda from Ruminantia. The most important differences are shown in
Table 2 and some are explained in several figures. The camelid stomach system differs from that of
ruminants. There are only three distinct forestomachs compared to four in ruminants. In camelids they
are called compartments (C) 1, 2 and 3. The rumen equivalent is C1, which possesses cranial and caudal
glandular sacs. These were once considered to represent the water store of the animal; however they
mainly function as absorption and fermentation areas as well as zones of enzymatic secretion (Wilson,
1989). The second, much smaller compartment C2 is the reticulum equivalent, and the eolongated C3 is
the combined omasum/abomasun equivalent, which might best be referred to as the tubular stomach
due to its length. Compartments 1 and 2 are lined with non-papillary smooth epithelium (Figure 1). In
camelids, the motility patterns are markedly different compared with ruminants. Another distinguished
feature of all Camelidae is the unique structure of their feet (Fig. 2). The padded feet act like snowshoes
allowing them to walk over soft, loose sand without sinking. Camelids walk on thick pads consisting
primarily of fat. They possess two digits, and their second and third phalanges are horizontal. The
reproductive physiology of camelids is of particular interest. Camels mate in a crouching position (Fig. 3)
and while mating the bull exteriorises its “doula” (Fig. 4), a bright pink inflatable sac, to attract females.
Camels are induced ovulators. Their gestation period lasted 13 months. A slippery surface of a third
membrane surrounding the fetus eases its birth (Figure 5). Latest osteological investigations on postcranial skeletons of Camelus dromedarius and C. bactrianus have shown that they derived from two
different ancestors. Approximately twenty million OWC exist, of which two million are Bactrians (Table 3).
There are four different species of NWC which inhabit the high altitudes in South America. The estimated
population of NWC is shown in Table 4. Llamas and alpacas were domesticated 7.000 years ago; the
dromedary and the Bactrian around 5.000 years ago. Guanacos and vicuñcas are wild and there are few
wild Bactrians which roam in the Chinese and Gobi desert. There are no wild dromedaries anymore. The
distribution of OWC is shown in Figure 6.
246
The knowledge of the susceptibility and resistance to infectious and parasitic diseases is of paramount
importance in an area where tylopods mix with other livestock.
Review of findings on FMD in camelids
FMD remains the single most important animal disease, and OWC and NWC inhabit countries in North and
East Africa, the Middle and Far East as well as in South America where FMD is endemic. It has been
reported that dromedaries can contract the disease following experimental infection and via close contact
with FMD diseased livestock, yet do not present a risk in transmitting FMD to susceptible animals
(Kitching, 2002). Summarised results are presented in the following Tables 5 to 8 (Wernery and Kaaden,
2004). Only two reports exist of a natural infection. The execution of experimental infections is poor, and
therefore conclusions are questionable.
FMD serology and infection in Bactrian camels remains
questionable, with FMD diagnosis only being made by means of clinical observations.
Results of recent FMD experiments in dromedaries in Dubai with serotype 0
Two Holstein heifers of around 150 kg (6-8 months of age) and two castrated male dromedaries
(Camelus dromedarius) around 400-450 kg (7-10 years of age) were each inoculated subepidermolingually with 107.6 Tissue Culture Infectious Doses 50% (TCID50) of foot-and-mouth disease virus (FMDV)
type O UAE 7/99 in a volume of 0.5 ml (Fig. 7). While the heifers developed elevated body temperatures,
were drooling saliva and had typical vesicular lesions (Fig. 8) on the tongue within 24 hours, the two
dromedaries did not show any clinical signs of disease and had no vesicular lesions, even at the
inoculation site. Infectious FMDV and FMDV RNA were detected at relatively high levels in sera and nasal
and mouth swabs from the heifers, but no infectious FMDV or FMDV RNA were isolated in similar samples
from the two dromedaries (Fig. 9). Furthermore, the two dromedaries did not develop any detectable
antibodies to FMDV. Based on the overall results obtained, we conclude that dromedaries (Camelus
dromedarius) are not susceptible to infection with this isolate of FMDV (Wernery et al., 2005).
Conclusion
Camelids belong to the suborder Tylopoda; they are not ruminants. Camelids possess a low flow
susceptibility to FMD, and do not appear to be long-term carriers of the FMDV. These are the main two
reasons to remove them from the OIE chapter as possessing the same degree of susceptibility as cattle,
sheep and goats.
References
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Zagazig, Egypt
Farag, M.A., Al-Sukayran, A., Mazlou, K.S, Al-Bokney, A.M., 1998. The susceptibility of camels to
natural infection with foot and mouth disease virus. Assiut Veterinary Medical Journal 40, 201 – 211
Fowler, M. E. (1997), Evolutionary history and differences between camelids and ruminants, J. Camel
Pract. and Research 4 (2), 99 – 105
Hafez, S.M., Farag, M.A., Al-Mukayel, Al, 1993. Are camels susceptible to natural infection with foot
and mouth disease virus? Internal Paper: National Agriculture and Water Research, Center Riyadh, Saudi
Arabia
Hedger, R.S., Barnett, I.T.R., Gray, D.F., 1980. Some virus diseases of domestic animals in the
Sultanate of Oman. Tropical Animal Health and Production 12, 107 –114
Kitching, P. (2002). Identification of foot and mouth disease virus carrier and subclinically infected
animals and differentiation from vaccinated animals. Revue scientifique et technique. Foot and mouth
disease: facing the new dilemmas. OIE 21 (3), 531 - 538
Kumar, A., Prasad, S., Ahuja, K.L., Tewari, S.C., Dogra, S.C., Garb, D.N., 1983. Distribution pattern
of foot and mouth disease virus types in North-West India (1979 – 1981). Haryana Veterinarian 22, 28 –
30
Metwally, M.A., Moussa, A.A., Reda, J., Wahba, S., Omar, A., Daoud, A., Tantawi, H.H., 1986.
Detection of antibodies against FMDV in camels by using fluorescent antibody technique. Agricultural
Research Review 64, 1079 – 1084
Moussa, A.A., Daoud, A., Tawfik, S., 1979. Susceptibility of camel and sheep to infection with foot and
mouth disease virus. Agricultural Research Revision Egypt 57, 1 –19
Moussa, A., Nasser, M.I., Mowafi, L., Salah, A., 1986a. Occurrence of foot and mouth disease in
different species of mammals at Sharkia province. Journal of Egypt Veterinary Medicine Association 40,
23 – 35
247
Moussa, A.A., Tantawi, H.H., Metwally, N.A., Wahba, S., Hussein, K., Osman, O.A., Saber, M.S.,
1986b. Pathogenicity of foot and mouth disease virus isolated from experimentally infected camels to
susceptible steers. Agricultural Research Review 64, 1071 – 1077
Moussa, A.A.M., Daoud, A., Omar, A., Meetwally, N., El-Nimr, M., McVicar, J.W. 1987. Isolation of
foot and mouth disease virus from camels with ulcerative disease syndromes. Journal of Egypt Veterinary
Medicine Association 47, 219 – 229
Moussa, A.A.M., 1988. The role of camels in the epizootiology of FMD in Egypt. In: FAO. The Camel:
Development Research. Proceedings of Kuwait Camel Seminar, Kuwait, Oct. 20 – 23, 1986, pp. 162 –
173
Moussa, H.A.A., Youssef, N.M.A., 1998. Serological screening for some viral diseases antibodies in
camel sera in Egypt. Egypt Journal of Agricultural Research 76, 867 – 873
Nasser, M., Moussa, A.A., Metwally, M.A., Saleh, R.EL.S., 1980. Secretion and persistence of foot
and mouth disease virus in faeces of experimental infected camels and ram. Journal of Egypt Veterinary
Medicine Association 40, 3 – 13
Paling, R.W., Jerset, D.M., Heath, B.R., 1979. The occurrence of infectious diseases and mixed
farming of domesticated and wild herbivores and domesticated herbivores including camels, in Kenya I.
Viral diseases: a serological survey with special reference to foot and mouth disease. Journal of Wildlife
Diseases 15, 351 – 359
Richard, D., 1979. Etude de la pathologie du dromedaire dans la souprovence du Borana (Ethiopie)
(Study of the pathology of the dromedary in Borana Awraja, Ethiopia). These Doctorales Veterinaire,
Paris No. 75, pp. 181 – 190
Wernery, U. and O.-R. Kaaden (2002). Infectious diseases in camelids, Blackwell Science, pp. 3 –17
Wernery, U. and O.-R. Kaaden (2004). Foot-and-mouth disease in camelids: a review, The Veterinary
Journal
Wernery, U., P. Nagy, C. M. Amaral-Doel, Z. Zhang and S. Alexandersen (2005). Dromedaries
(Camelus dromedarius) appear not to be susceptible to infection with foot-and-mouth disease virus
serotype 0, The Vet. Rec. (in press)
Wilson, R. T. (1989). Ecophysiology of the camelidae and desert ruminants, Springer Verlag, pp. 96 –
98
248
Table 1: Classification of camelids and other artiodactylids (Wernery and Kaaden, 2002)
Class
Mammalia
Order
Artiodactyla
Suborder
Suiformes
Hippopotamuses, swine, peccaries
Suborder
Tylopoda
Camelids
Old
Camelus dromedarius – dromedary camel
World
Camelus bactrianus – Bactrian camel
Lama glama – llama
New
Lama glama – llama
World
Lama pacos – alpaca
Lama guanicoe – guanaco
Vicugna vicugna – vicuña
Suborder
Ruminantia
Cattle, sheep, goats, water buffalo, giraffe, deer, antelope, bison
249
Table 2: Differences between camelids and ruminants
Camelids
Evolutionary pathways diverged 40 million
years ago
Ruminants
Evolutionary pathways diverged 40 million
years ago
Blood
•
red blood cells elliptical and small
(6.5 µ)
•
predominant white blood cell is the
neutrophil
Foot
•
has toenails and soft solar pad
•
second and third phalanges are
horizontal
Digestive System
•
foregut fermenter, with
regurgitation, re-chewing and reswallowing
•
stomach – 3 compartments (C1-3),
resistant to bloat
•
compartment 1 and 2 have stratified
squamous epithelium
•
2 glandular sacs in C1, act as
“reserve water tanks”
Reproduction
•
induced ovulator
•
no oestrus cycle
•
follicular wave cycle
•
copulation in prone position
•
diffuse placentation
•
epidermal membrane surrounding
fetus
•
cartilaginous projection on tip of
penis
•
ejaculation prolonged
Urinary
•
smooth and elliptical kidney
•
suburethral diverticulum in female at
external urethral orifice
•
dorsal urethral recess
Blood
•
red blood cells round and larger (10
µ)
•
predominant white blood cell is the
lymphocyte
Foot
•
has hooves and sole
•
second and third phalanges are
nearly vertical
Digestive System
•
same (parallel evolution)
Parasites
•
unique lice and coccidia
•
share some gastrointestinal
nematodes with cattle, sheep and
goats
Infectious diseases
•
minimally susceptible to tuberculosis
•
bovine brucellosis is rare
•
mild susceptibility to foot-and-mouth
disease
•
rarely
develop
clinical
disease
following exposure/inoculation with
other bovine and small ruminant viral
diseases
Parasites
•
unique lice and coccidia
•
share gastrointestinal nematodes
•
•
stomach – 4 compartments,
susceptible to bloat
rumen has papillary epithelium
•
no glandular sacs
Reproduction
•
spontaneous ovulation
•
oestrous cycle
•
no follicular wave cycle
•
copulation in standing position
•
cotyledonary placentation
•
no epidermal membrane surrounding
fetus
•
no cartilaginous projection on tip of
penis
•
ejaculation short and intense
Urinary
•
smooth or lobular kidney
•
no suburethral diverticulum
•
dorsal urethral recess in some
species
Infectious diseases
•
Highly susceptible to tuberculosis,
bovine brucellosis and foot-andmouth disease
250
Table 3: Old World camel population in Africa and Asia
Africa
Camel
Asia
Population
Camel
Population
Algeria
150,000
Afghanistan
270,000
Chad
446,000
India
1,150,000
Djibouti
60,000
Iran
27,000
Egypt
90,000
Iraq
250,000
Ethiopia
1,000,000
Israel
11,000
Kenya
610,000
Jordan
14,000
Libya
135,000
Kuwait
5,000
Mali
173,000
Mongolia
580,000
Mauritania
800,000
Oman
6,000
Morocco
230,000
Pakistan
880,000
Niger
410,000
Qatar
10,000
Nigeria
18,000
Saudi Arabia
780,000
Senegal
6,000
Syria
7,000
Somalia
6,000,000
Turkey
12,000
Sudan
2,600,000
United Arab
120,000
Emirates
Tunisia
173,000
Yemen
210,000
Upper Volta
6,000
IPS*
200,000
Western
92,000
China
600,000
Australia
120,000
Canary
4,000
Sahara
Islands
Total
12,999,00
Total
5,256,000
0
Grand Total
18,255,000
* Independent States of the Soviet Union
251
Table 4: Estimated population of South American camelids
Country
Llamas
Alpacas
Guanacos
Vicuñas
Argentina
75,000
2,000
550,000
23,000
Bolivia
2,500,000
300,000
?
12,000
Chile
85,000
5,000
20,000
28,000
Peru
900,000
3,020,000
1,400
98,000
Australia
< 5,000
> 5,000
A few in zoos
0
Canada
> 6,000
> 2,000
< 100 in zoos
> 10
Europe
< 2,000
< 1,000
< 100 in zoos
< 100 in
zoos
United States
> 110,000
> 9,500
145, mostly in
0
zoos
In
ISIS
343
303
397
100
Total
3,683,343
3,344,803
572,142
161,210
Grand Total
7,761,498
registry
in
zoos*
* ISIS = International Species Inventory System
Table 5: FMD in New World Camelids
FMD Serology:
Field investigations. Reliable serological tests are available
So far all investigations are negative despite NWC mixing with FMD positive contact
animals
Experimental investigations
Antibodies have been produced to FMD using different routes and serotypes
FMD Infection:
Field investigations
One case in alpacas showing minor disease, but no virus isolated
Experimental investigations
NWC can be infected with different serotypes and demonstrate mild to severe clinical
signs. Virus can also be transmitted to other susceptible animals. FMDV was not
isolated after 14 days. No carriers?
252
Table 6: Reports on dromedary FMD-antibodies from field surveys
Authors
Year
Country
Serotypes
Richard
Hedger et al.
Moussa et al.
Paling et al.
1979
1980
1986a
1979
Kenya
Oman
Egypt
Nigeria
Abou-Zaid
1991
Egypt
Hafez et al.
Hafez et al.
1993
1993
Moussa+Youssef
Farag et al.
1998
1998
Wernery
comm.
Younan
comm.
pers.
2003
Egypt
Saudi
Arabia
Egypt
Saudi
Arabia
U.A.E.
pers.
2003
Kenya
*
**
***
Positive
%
2.6
nil
5.4
nil
nil
10.6
23.5
nil
nil
Test
Endemic
A,O,SAT1,2
A,O,C,SAT1,Asia1
O
C,O,SAT2
O
O
O
O
O
Sera
tested
87
203
1755
88
536
536
536
364
650
VNT*
VNT
VNT
VNT
AGID**
ICFT***
ELISA
VNT
VNT
yes
yes
yes
yes
O
A,O
169
25
24.3
nil
yes
yes
O
374
nil
ELISA
VNT,
AGID
ELISA
O
324
nil
ELISA
yes
yes
yes
yes
yes
Virus Neutralisation Test
Agargel Immunodiffusion Test
Indirect Complement Fixation Test
Table 7: Seroconversion in dromedaries after inoculation with FMDV
Author
Year
Country
Moussa et
al.
Nasser et
al.
Metwally
et al.
Moussa
1979
Egypt
Dromedaries
tested
5
1980
Egypt
2
1986
Egypt
2
1988
Egypt
?
1991
Saudi
Arabia
?
3
AbouZaid
Hafez
al.
et
1993
Method
Result
5/5
0/5
intransal
SNT*
AGID
Not done
intranasal
FAT**
intranasal
SNT
01/2/72
Egypt
intranasal
01/3/87
Egypt
intradermolingual
01/2/72
Egypt
01/2/72
Egypt
01/2/72
Egypt
0
Inoculation
Route
intranasal
Egypt
1
*
**
***
Serotype
01/3/87
Egypt
footpad
Duration of
antibodies
nil
?
6 weeks
?
?
2/2 low
titres
positive
low
Nil
SNT
ICFT***
3/3
3/3
10 weeks
6 weeks
AGID
ELISA
0/3
3/3
nil
11 weeks
SNT
ICFT
0/1
0/1
nil
nil
AGID
ELISA
0/1
0/1
nil
6 weeks
3 months
nil
Serum Neutralisation Test
Fluorescence Antibody Test
Indirect Complement Fixation Test
253
Table 8:
Reports on experimental FMD infection and virus isolation from field cases
Authors
Year
Country
Egypt
Mode of
infection
Intranasal
Dromedaries
tested
5
Moussa et
al.
Nasser et
al.
Metwally
et al.
Moussa et
al.
Hafez et
al.
AbouZaid
1979
1980
Egypt
Intranasal
2
1986
Egypt
i.v.
2
1986
b
1993
Egypt
Intradermolingual
5
Saudi
Arabia
Intranasal
?
1991
Egypt
Kumar et
al.
Moussa et
al.
1983
India
Intradermolingual
Footpad
Natural
3
1
2
1987
Egypt
Natural
4
0
Farag
al.
1998
Saudi
Arabia
Natural
30
nil
et
Serotype
01/2/72
Egypt
01/2/72
Egypt
01/2/72
Egypt
01/2/72
Egypt
01/2/72
Egypt
01/2/87
Egypt
0
Clinical
signs
nil
nil
Virus
reisolation
1-4
weeks
OPF
1-6 days
faeces
1-3 weeks
nil
Blood
nil
?
yes
Blood, OPF,
faeces
Negative
Tongue/gum
from one
Ulcers
nil
nil
?
Vesicles
ulcers
swelling
of limbs
nil
Probang
254
Figure 1: The forestomach system of Tylopoda
DGS
C1
C2
DU
VGS
C3
DGS = dorsal glandular sac; VGS = ventral glandular sac; C1 = compartment 1 (rumen)
C2 = compartment 2 (reticulum); C3 = compartment 3 (tubular stomach); DU = duodenum
Figure 2: Feet of a llama and a dromedary
255
Figure 3: Mating camels
Figure 4: The rutting bull inflates and exteriorises its “doula”
256
Figure 5: A slippery third membrane surrounds the newborn calf
Figure 6: Distribution of C. dromedarius and C. bactrianus
C. dromedarius
C. bactrianus
257
C. dromedarius introduced
Figure 7:
Subepidermolingual FMDV-inoculation of a dromedary
Figure 8:
Typical FMD lesions on the tongue of a heifer three days after
subepidermolingual inoculation
258
Figure 9:
Probang sampling of a dromedary
259