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Research in Veterinary Science 92 (2012) 351–355

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Research in Veterinary Science


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Brucellosis in camels
Mayada Gwida a,b,⇑, Adel El-Gohary b, Falk Melzer a, Iahtasham Khan a, Uwe Rösler c, Heinrich Neubauer a
a
Friedrich-Loeffler Institut, Institute for Bacterial Infections and Zoonoses, Jena, Germany
b
Department of Hygiene and Zoonoses, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
c
Freie Universität Berlin, Institute, of Animal and Environmental Hygiene, Berlin, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Camels are highly susceptible to brucellosis caused by Brucella melitensis and Brucella abortus. Difficulties
Received 13 August 2010 can arise in diagnosis of camel brucellosis, especially as this disease provokes only few clinical signs in
Accepted 3 May 2011 contrast to its clinical course in cattle. Because none of the commonly used serological test can be per-
ceived as a perfect test for Brucella diagnosis in camel and most serological tests used for camels have
been directly transposed from cattle without adequate validation, an incorrect diagnosis may occur when
Keywords: diagnosis is based on serology alone. Of imminent concern is the fact that brucellosis can be easily trans-
Brucellosis
mitted from animals or their products to humans mainly via milk. In many developing countries in the
Camels
Epidemiology
arid areas of Asia and Africa, camels are still the most important productive livestock for nomadic pop-
Public health importance ulations. Therefore, we reviewed the literatures on camel brucellosis to highlight the epidemiologic, eco-
nomic and public health impact of camel brucellosis as a basis for designing effective control strategies.
Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction communities in diverse ecozones throughout the world are


depending on camels for their livelihood. This dependence consists
Camelids are members of the biological family Camelidae, came- of utilization of camel meat, milk, leather and wool, exportation of
lids are classified in the suborder Tylopoda (pad-footed animals) live camels, uses as an important sport and tourism resource in the
that represents with the suborders Suiformes (pig-like) and Rumi- Arabian Gulf countries and lastly the use of camels as animals for
nantia (ruminants) the order Artiodactyla (even-toed ungulates) packing, transport and riding (Wilson, 1984; Rollefson, 2000). In
(Schwartz and Dioli, 1992). The family Camelidae is divided into their natural desert habitat where camels are usually raised partic-
two genera: The genus camelus, old-world genus, includes two spe- ularly during the long dry season, camels are subjected to severe
cies: Camelus dromedarius, the dromedary, one-humped or Arabian stress conditions which render them susceptible to many diseases
camel; and the Camelus bactrianus, the bactrian or the two-humped and ailments (Abbas et al., 1993; Agab, 1993). Although camels
camel and the new world camels (genus Lama with the species L. were considered in the past, and for a fairly long time, as resistant
glama, L. guanicoe, L. pacos and genus Vicugna with the species V. vic- to many disease causing factors (Zaki, 1948; Dalling et al., 1988),
ugna) (Wilson and Reeder, 2005). The habitat of the dromedary is it has been proved that they are susceptible, the same as other live-
the dry hot zones of North Africa, Ethiopia, the Near East and West stock or even more, to the common disease causing pathogens
Central Asia. Bactrian camel occupies the cold deserts of southern affecting other animal species (Wilson 1984; Abbas and Tilley,
areas of the former Soviet Union, Mongolia, East-Central Asia and 1990; Abbas and Agab, 2002).
China (Wilson, 1984). The limeades exist in the cold heights of Latin Brucellosis is a serious zoonotic disease affecting man and all
America. It is believed that the dromedary camel was first domesti- domestic animals including camels. It is considered as one of the
cated in Southern Arabia (Zeuner, 1963) or in the Northern steppe great public health problem all over the world (Radostits et al.,
and deserts of Arabia (Bullet, 1975). The camel plays vital socio- 2007). However, camel brucellosis has not received proper atten-
economic roles and supports the survival of millions of people in tion from researchers and scientists. Brucellosis was reported in
the semi dry and arid zones of Asia and Africa. It has been found that camels as early as 1931 (Solonitsuin, 1949); since then, the disease
camels are the fit domestic animal during severe drought periods. has been reported from all camel-keeping countries (Table 1). Cam-
The camel not only survived such droughts, but continued produc- els are not known to be primary hosts of Brucella, but they are sus-
ing and reproducing (Schwartz, 1992). Many pastoral groups and ceptible to both B. abortus and B. melitensis (Cooper, 1991).
Consequently, the prevalence depends upon the infection rate in
⇑ Corresponding author at: Department of Hygiene and Zoonoses, Faculty of primary hosts being in contact with them. Since Brucella species
Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt. were isolated from camels (Table 2), consumption of milk and meat
E-mail address: mayadam_rah@yahoo.com (M. Gwida). has led to a high number of human brucellosis cases and thus

0034-5288/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.rvsc.2011.05.002
352 M. Gwida et al. / Research in Veterinary Science 92 (2012) 351–355

Table 1
Summary of literature regarding the occurrence of antibodies to Brucella in camels.

Country Number Positive % Test References


Egypt 200 20.0 SAT (serum agglutination test) Zaki 1948
175 10.3 SAT Hamada et al. (1963)
780 23.3 TAT (tube agglutination test) Salem et al. (1990)
13.9 CFT (complement fixation test)
13.5 2 MET (mercaptoethanol test)
8.2 RBT (rose bengal test)
360 11.5 TAT, RBT Nada and Ahmed (1993)
500 7.0 RBT El-Sawalhy et al. (1996)
2.3 cELISA (competitive enzyme linked
immunosorbent assay)
592 1.0 STAT (standard tube agglutination test) Abou-Eisha (2000)
1.7 Card test
766 8.7 RBT Abdel Moghney (2004)
9.3 ELISA (enzyme linked iimmunosorbent assay)
340 7.4 CFT EL-Boshy et al. (2009)
Libya 967 4.1 RBT, SAT, CFT Gameel et al. (1993)
520 1.4 RBT Azwai et al. (2001)
1.2 SAT
3.0 cELISA
Sudan 740 4.9 RBT, SAT, CFT Abu-Damir (1984)
238 3.0 SAT Abbas et al. (1987)
38 84.2 RBT Agab et al. (1994)
64 0 SAT & TAT El-Ansary et al. (2001)
3274 7.8 RBT, SAT & CFT Musa and Shigidi (2001)
29 13.8 ? cELISA
10.3 ? RBT
3549 30.5 RBT Omer et al. (2007)
21 23.8 RBT & SAT Musa et al. (2008)
Ethiopia 1442 5.7 RBT Teshome et al. (2003)
Nigeria 232 1 RBT & SAT Okoh (1979)
329 11.4 (RBT, SAT, cELISA) Junaidu et al. (2006)
480 7.5 MSAT (microtitre serum agglutination test) Kudi et al. (1997)
Somalia 913 1.9 SAT Baumann and Zessin (1992)
0.3 CFT
1246 3.9 RBT Ghanem et al. (2009)
3.1 iELISA (indirect enzyme linked immunosorbent
assay)
Kenya 172 6.4 RBT, SAT Waghela et al. (1978)
12.2 CFT
Jordan 412 12.1 RBT, CFT Al-Majali et al. (2008)
640 14.2 RBT Dawood (2008)
Saudi Arabia 146 1.4 RBT Hashim et al. (1987)
2630 8 RBT, SPA (standard plate agglutination test) Radwan et al. (1992)
236 8 RBT Radwan et al. (1995)
98 7.1 RBT, SAT Hegazy et al. (2004)
859 1.86 RBT Alshaikh et al. (2007)
3.03 cELISA
Republic of Yemen 105 0.0 ELISA AL-Shamahy (1999)
Kuwait 698 14.8 RBT, CFT AL-Khalaf and EL-Khaladi (1989)
Abu Dhabi 392 1.0 RBT Afzal and Sakkir (1994)
1.5 SA (standard agglutination)
1794 5.8 ? (1990–1991) RBT Moustafa et al. (1998)
7899 0.1 ? (1995–1996) RBT Moustafa et al. (1998)
Iran 953 8.0 RBT, SAT, CFT, 2MET Zowghi and Ebadi (1988)
258 1.9 RBT, SAT, 2MET Khadjeh et al. (1999)
1123 10.5 RBT Ahmad and Nemat (2007)
Pakistan 81 2.5 STA Ajmal et al. (1989)
71 8.0 Straten et al. (1997)

serious public health concern has aroused (Kiel and Khan, 1989). nomic and public health impact of camel brucellosis as a basis for
This high number can be farmers from nomadic areas believe that designing effective control strategies.
raw camel milk has a curative effect on their digestive system.
The epidemiology of brucellosis in cattle and small ruminants at
different geographical areas has been investigated extensively. In 2. Economic importance of camels
spite of its vital importance, studies on this disease in camels are
scarce due to the fact that camel production in remote area coin- Camels play an important socio-economic role within the pas-
cides with poor infrastructure (Schwartz and Dioli, 1992). Difficul- toral and agricultural system in dry and semi dry zones of Asia
ties can arise in diagnosis of camel brucellosis, especially as this and Africa. The camel possesses unique qualities which make it
disease provokes only few clinical signs in contrast to its clinical superior to other domesticated animals in the hot and arid desert
course in cattle (Mousa et al., 1987). Therefore, we reviewed the lit- ecosystems where they contribute to the desertification combat
erature on reports camel brucellosis to highlight epidemiology, eco- and food security. Camels are also still an important means of
M. Gwida et al. / Research in Veterinary Science 92 (2012) 351–355 353

Table 2
Brucella species isolated from camels.

Country Brucella species Organ culture References


Sudan Brucella melitensis biotype 3 Lymph nodes Agab et al. (1996)
Brucella melitensis biotype 3,6 Lymph node Musa et al. (2008)
Jordan Brucella melitensis biotype 3 Aborted fetuses, milk Dawood (2008)
Iran Brucella melitensis biotype 1 Lymph node Zowghi and Ebadi (1988)
Brucella melitensis biotype 1 Lymph node Khadjeh et al. (1999)
Kuwait Brucella abortus biotype 1 Foetal stomach contents Al-Khalaf and El Khaldi (1989)
Libya Brucella melitensis biotype 1 Milk, aborted foetus, vaginal swab Gameel et al. (1993)
Egypt Brucella melitensis biotype 3 Milk Abou-Eisha (2000)

draught and transport for pastoral societies (Schwartz and Dioli, 3. Public health importance of brucellosis
1992). They serve as a cheap source of power for drawing water
from wells, plowing and leveling land, working mini mills for oil Human brucellosis is a potentially life-threatening multisystem
extraction (from oil seeds), grinding wheat, corn and other grains disease with a broad spectrum of nonspecific symptoms (Makis
and for crushing sugarcane, and pulling carts for the transportation et al., 2008). Brucellosis in humans is a major public health hazard
of goods as well as people (Yaqoob and Nawaz, 2007). Additionally, which affects social and economic development in various coun-
camel milk is one of the most valuable food resources for nomads tries due to acute and chronic illness, physical incapacity and loss
in arid regions and increases the income of pastoralists. Camel milk of manpower (Corbel, 2006). Occupational acquired brucellosis is
possesses superior storage life in comparison to cow milk due to its of special concern for public health because of the high risk of
high content of proteins having inhibitory effect on bacteria (Farah direct transmission from infected animals to persons being em-
et al., 2004). It was confirmed that camel milk has special medici- ployed in animal husbandry. This exposed group includes slaugh-
nal properties, especially for dropsy, jaundice and conditions ter men, dairymen, herdsmen and veterinary clinicians.
affecting the lungs and spleen (Seifu, 2007). The positive effect of Herdsmen are at the highest risk. The occupational exposure is
camel milk on diabetic patients has been studied in India the con- high especially in countries where herding of animals is still tradi-
sumption of 0.5 l of camel milk per day, the insulin demand de- tional and unscientific (Straten et al., 1997). Camels’ milk is
creased in diabetic patients and glycaemia was better balanced increasingly becoming a delicacy, as in Arab nations camel milk
(Agrawal et al., 2005). In part of Ethiopia, camel milk is considered is consumed raw by camel keeper. Isolation of B. melitensis from
to have an aphrodisiac effect (Knoess, 1984). camels’ milk (Gameel et al., 1993) and seropositivity to B. abortus
Besides milk, meat is one of the most important products from and B. melitensis indicate that brucellosis is a hazard to public
camels. Yield and quality of the carcasses are comparable to other health. Therefore, pasteurization is adequate for public health
livestock. However, camels are still not systemically bred for meat assurance especially the pasteurization does not affect the chemi-
production as they are considered too valuable for this production cal composition of camel milk Farah (1996).
type. Another important product is camel hair. It is one of the Human infection due to Brucella from camels is known to occur
world’s most expensive natural animal fibers. Camelids are appre- mostly through the consumption of raw milk (Kiel and Khan,
ciated for the high quality of their wool (alpaca and Bactrian ca- 1989). Malta fever due to B. melitensis was diagnosed in 30% of
mel). Recently, the camel leather industry was better valorized in the camel handlers and milkers on large camel farm in Riyadh, Sau-
relationship with the touristic activities. Camel hides are known dia Arabia. The abortion rate in the farm reaching 12% and B. mel-
for their strength and durability. They are used by camel breeders, itensis biovars 1, 2 and 3 were isolated from aborted camel fetuses
but also for fashion accessories (Wernery, 2003). Other products Radwan et al. (1995). Therefore, there is a real need for cooperation
used are dung as fertilizer and as a source of fuel for pastoralists. between public health officials and veterinary officers to reduce
Bones are used for production of jewellery or bone-meal for fertil- the circulation of human brucellosis in endemic areas (Jelastopulu
izing purposes (Rollefson, 2000). No doubt, camel can be a tool to et al., 2008).
combat the future challenges of draught, environmental changes,
global warming and threats of new disease. Camel is the animal
of future, i.e. everlasting threat to the environment, global warm- 4. Clinical signs
ing, creeping desertification and competition on feed and water re-
sources are the future challenges which can be beat by camel only. Camels of both species (C. dromedarius and C. bactrianus) are fre-
Camel has a good potential as meat export. Camel meat is pro- quently infected with Brucella organisms, especially when they are
duced organically and is free of zoonotic diseases like mad cow dis- in contact with infected large and small ruminants (Radwan et al.,
ease, swine flu and avian influenza. Its physiology and special 1992). Serological evidence for Brucella infection in camels has
features are therefore not only of a scientific interest, but are the been reported from Asia and Africa (Table 1). Non pregnant drom-
basic sustenance for people who live in marginal dry land areas edaries experimentally infected with a field strain of B. abortus
(Wardeh, 2004). The new trends to improve camel production developed only mild, transient clinical symptoms including re-
can occur through, intensification of camel production by the duced appetite, slight lameness and bilateral lacrimation (Abu Da-
development of modern dairy farms with high dairy potential lac- mir et al., 1989). Orchitis and epididymitis have also been
tating camels and industrial milk processing (pasteurized milk, associated with brucellosis caused by B. abortus and B. meletensis
cheese making, and modern packaging), or camel feed-lot with (Tibary et al., 2006). Other conditions caused by the disease were
intensification of the reproduction process; trials to diversify camel retention of placenta, placentitis, uterine infections, fetal death
production with increasing its use in agriculture activities, carting, and mummification, delayed maturity and infertility; it also caused
leisure (mainly for small camelids), increasing demand of camel arthritis and hygroma (Ramadan et al., 1998; Tibary et al., 2006;
milk and meat for dietetic and medicinal purposes (Mehari et al., Ahmad and Nemat, 2007; Musa et al., 2008). As previously men-
2007). tioned, abortion has been reported in pregnant camels and B. mel-
354 M. Gwida et al. / Research in Veterinary Science 92 (2012) 351–355

itensis was isolated from aborted foetuses, genital discharge, urine Immunosorbent Assay (cELISA), and Mercapto-ethanol test (2ME)
and milk Radwan et al. (1995). Moreover, different biovars of B. for the diagnosis of camel brucellosis (Azwai et al., 2001; Abdel
melitensis were isolated from camel milk (Radwan et al., 1992; Ga- Moghney, 2004; Alshaikh et al., 2007). With the development of
meel et al., 1993; Abou-Eisha, 2000; Hamdy and Amin, 2002) commercial camel dairies in several countries, this disease should
which indicates that this organism is excreted through milk. How- be seriously considered because of its impact on human health.
ever, the clinical signs were milder and the antibody concentra- Unfortunately, till now, there are no studies on vaccination or
tions were lower in camels than in cattle (Musa et al., 1990). eradication strategies of camel brucellosis (Tibary et al., 2006).
However, the options to control brucellosis included immuniza-
tion, testing and removal, and improving management practices
5. Epidemiology of camel brucellosis and movement control (WHO, 1997; Wernery and Kaaden 2002).
Control of camel brucellosis should suite the conditions of the par-
Brucellosis in animals causes tremendous economic losses due ticular country where camels are raised. Vaccination of uninfected
to abortion, premature birth, decreased milk production, reduced animals is generally considered the most effective and economical
fertility and cross transmission to other animal species, the zoo- means of protecting livestock against brucellosis. Consequently,
notic potential of the disease in camels should not be overlooked. vaccination was performed on all negative reactors immediately
Despite the advances made in surveillance and control, the preva- after the third serological testing, to avoid the possible presence
lence of brucellosis is increasing in many developing countries due of carrier animals (Radwan et al., 1995). In most of the developing
to various sanitary, socioeconomic, and political factors (Pappas countries by pastoralists, brucellosis prevalence is low. Thus con-
et al., 2006). Brucellosis is caused by Gram negative coccobacilli trol by herd immunization and vaccination of calves at 4 to
of the genus Brucella which are facultative intracellular. They can 8 months of age is helpful using S19 or Rev 1 vaccinal strains
survive within host cells causing a chronic disease that may persist preceded by blood testing using the SAT or card test on the field.
throughout the life time of the animal. Camels can be infected by B. Seropositive animals should be identified and subjected to
abortus and B. melitensis. The appearance of brucellosis depends on retesting. Additionally, test and slaughter policy can be followed
the Brucella species being prevalent in other animals sharing their in countries where intensification is practiced (Abbas and Agab,
habitat (cross transmission between species) and on the husbandry 2002).
system (Musa et al., 2008). A close contact between infected and In conclusion, camels play an importance role in the epidemiol-
susceptible camels in a herd promotes the spread of diseases. ogy of brucellosis; the possibility that brucellosis may spread from
The camels are always herded together with sheep and goats and camels, especially through milk and the lack of current and de-
to a lesser extent with cattle and they share the same watering tailed epidemiological study of the disease in camels strongly calls
points and pastures, and so it is not surprising to find a higher for a reassessment of the prevalence of the disease. This will allow
incidence of the disease among camels (Teshome et al., 2003). an effective control program to be designed and serve as a baseline
The differences in the prevalence of camel brucellosis from differ- for further research.
ent countries may be attributed to varying husbandry and manage-
ment practices, the number of susceptible camels, the virulence of
the organisms, presence of reactor animals in the region, absence References
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