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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 re-assessed. 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 post-cranial 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.
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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 subepidermo-lingually 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 Abou Zaid, A.A., 1991. Studies on some diseases of camels. PhD Thesis, Faculty of Veterinary Medicine 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
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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
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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
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Table 2: Differences between camelids and ruminants Camelids Ruminants Evolutionary pathways diverged 40 million years ago
Evolutionary pathways diverged 40 million years ago
Blood Blood
• red blood cells elliptical and small (6.5 µ)
• predominant white blood cell is the neutrophil
• red blood cells round and larger (10 µ)
• predominant white blood cell is the lymphocyte
Foot • has toenails and soft solar pad • second and third phalanges are
horizontal
Foot • has hooves and sole • second and third phalanges are
nearly vertical Digestive System Digestive System
• foregut fermenter, with regurgitation, re-chewing and re-swallowing
• 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”
• same (parallel evolution) • stomach – 4 compartments,
susceptible to bloat • rumen has papillary epithelium • no glandular sacs
Reproduction 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
• 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 and elliptical kidney • suburethral diverticulum in female at
external urethral orifice • dorsal urethral recess
Urinary • smooth or lobular kidney • no suburethral diverticulum • dorsal urethral recess in some
species
Parasites • unique lice and coccidia • share some gastrointestinal
nematodes with cattle, sheep and goats
Parasites • unique lice and coccidia • share gastrointestinal nematodes
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
Infectious diseases • Highly susceptible to tuberculosis,
bovine brucellosis and foot-and-mouth disease
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Table 3: Old World camel population in Africa and Asia
Africa Camel
Population Asia
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
Emirates
120,000
Tunisia 173,000 Yemen 210,000
Upper Volta 6,000 IPS* 200,000
Western
Sahara
92,000 China 600,000
Australia 120,000
Canary
Islands
4,000
Total 12,999,00
0
Total 5,256,000
Grand Total 18,255,000
* Independent States of the Soviet Union
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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
zoos
0
In ISIS
registry in
zoos*
343 303 397 100
Total 3,683,343 3,344,803 572,142 161,210
Grand Total 7,761,498
* 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?
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Table 6: Reports on dromedary FMD-antibodies from field surveys Authors Year Country Serotypes Sera
tested Positive %
Test Endemic
Richard 1979 Kenya A,O,SAT1,2 87 2.6 VNT* yes Hedger et al. 1980 Oman A,O,C,SAT1,Asia1 203 nil VNT yes Moussa et al. 1986a Egypt O 1755 5.4 VNT yes Paling et al. 1979 Nigeria C,O,SAT2 88 nil VNT yes O 536 nil AGID** Abou-Zaid 1991 Egypt O 536 10.6 ICFT*** O 536 23.5 ELISA
yes
Hafez et al. 1993 Egypt O 364 nil VNT yes Hafez et al. 1993 Saudi
Arabia O 650 nil VNT yes
Moussa+Youssef 1998 Egypt O 169 24.3 ELISA yes Farag et al. 1998 Saudi
Arabia A,O 25 nil VNT,
AGID yes
Wernery pers. comm.
2003 U.A.E. O 374 nil ELISA yes
Younan pers. comm.
2003 Kenya O 324 nil ELISA yes
* Virus Neutralisation Test ** Agargel Immunodiffusion Test *** Indirect Complement Fixation Test Table 7: Seroconversion in dromedaries after inoculation with FMDV
Author Year Country Dromedaries tested
Serotype Inoculation Route
Method Result Duration of antibodies
Moussa et al.
1979 Egypt 5 01/2/72 Egypt
intranasal SNT* AGID
5/5 0/5
nil
Nasser et al.
1980 Egypt 2 01/2/72 Egypt
intransal Not done ?
?
Metwally et al.
1986 Egypt 2 01/2/72 Egypt
intranasal FAT** 2/2 low titres
6 weeks
Moussa 1988 Egypt ? 0 intranasal SNT positive low
3 months
Abou-Zaid
1991 Saudi Arabia
? 01/2/72 Egypt
intranasal ? Nil nil
SNT 3/3 10 weeks 3 01/3/87
Egypt intrader-molingual
ICFT*** 3/3 6 weeks
AGID 0/3 nil Hafez et al.
1993 Egypt ELISA 3/3 11 weeks
SNT 0/1 nil 1 01/3/87
Egypt footpad ICFT 0/1 nil
AGID 0/1 nil ELISA 0/1 6 weeks
* Serum Neutralisation Test ** Fluorescence Antibody Test *** Indirect Complement Fixation Test
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Table 8: Reports on experimental FMD infection and virus isolation from field cases
Authors Year Country Mode of infection
Dromedaries tested
Serotype Clinical signs
Virus re-isolation
Moussa et al.
1979 Egypt Intranasal 5 01/2/72 Egypt
nil 1-4 weeks OPF
Nasser et al.
1980 Egypt Intranasal 2 01/2/72 Egypt
nil 1-6 days faeces
Metwally et al.
1986 Egypt i.v. 2 01/2/72 Egypt
nil 1-3 weeks
Moussa et al.
1986 b
Egypt Intradermolingual 5 01/2/72 Egypt
nil Blood
Hafez et al.
1993 Saudi Arabia
Intranasal ? 01/2/72 Egypt
nil ?
Abou-Zaid
1991
Egypt
Intradermolingual
3
01/2/87 Egypt
yes
Blood, OPF, faeces
Footpad 1 nil Negative Kumar et al.
1983 India Natural 2 0 ? Tongue/gum from one
Moussa et al.
1987 Egypt Natural 4 0 Vesicles ulcers swelling of limbs
Ulcers
Farag et al.
1998 Saudi Arabia
Natural 30 nil nil Probang
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Figure 1: The forestomach system of Tylopoda 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
DGS
C1C2
C3
VGS
DU
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Figure 3: Mating camels
Figure 4: The rutting bull inflates and exteriorises its “doula”
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Figure 5: A slippery third membrane surrounds the newborn calf
Figure 6: Distribution of C. dromedarius and C. bactrianus
C. dromedarius C. bactrianus
C. dromedarius introduced
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Figure 7: Subepidermolingual FMDV-inoculation of a dromedary
Figure 8: Typical FMD lesions on the tongue of a heifer three days after
subepidermolingual inoculation
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Figure 9: Probang sampling of a dromedary