1. TAn Overview of the Equine and Camel Industry in Egypt
The estimated current sizes of the target animal populations in Egypt include 120,000 camels and 85,000 horses
[1][2][4,22].
1.1. Equines
About 230 farms in Egypt specialize in raising Arabian horses, and the Egyptian Agricultural Authority offers pedigree certifications for all horses sold to foreign nations that go back up to six generations, in addition to permanently marking all animals they possess (Freeze Marking). Also, a single office creates the formal documents required for export activities.
In Egypt, a number of horse breeders from various nations are invited to a competition that is held every year in the month of November. This event has a number of equestrian competitions and shows that are judged by an international committee. The organization of international festivals and contests that take place in Egypt has an important economic impact, since numerous visitors from foreign countries, including neighboring Arabic countries, are usually interested in attending these events, which also refreshes the tourist industry and drives horse trading
[3][23].
Additionally, in many rural areas of Egypt, horses, donkeys, mules, and ponies are often used as working equids. These animals assist personnel in a variety of sectors, including agriculture and construction, help farmers in soil drilling and public transportation, and contribute to sustaining the livelihoods of millions of people
[4][5][5,6].
1.2. Camels
Three species of camels can be found in Egypt: the one-humped Arabian camel [also known as dromedaries] (
Camelus dromedarius), the Bactrian camel (
Camelus bactrianus), which is a two-humped camel, and its wild counterpart (
Camelus ferus)
[6][7][8][9][19,24,25,26]. The one-humped camel
Camelus dromedarius, or dromedary, is a domestic animal belonging to the Camelidae family and is widely distributed in the arid and semi-arid regions of Africa, Arabia, and western Asia, extending up to India
[10][8]. The world’s current camel population is about 28 million heads, and 80% of them live in Africa, with 60% in the Horn of Africa. Arabian camels (Dromedaries) constitute 94% of the world’s camel population
[2][11][22,27]. In Egypt, there are four distinct camel breeds, belonging to Camelus dromedarius, which differ phenotypically: the Sudani (often used for riding and racing), the Falahi or Baladi (used for transportation and agricultural work), the Maghrabi (used for both meat and milk), and the Mowallad (a hybrid of the two)
[12][28].
Arabian camels significantly contribute to Egypt’s local economy and culture. They do so by producing milk and meat for human consumption, as well as wool. Regarding camel milk production, unfortunately in Egypt, camel milk is underestimated, and it does not seem to contribute significantly to the economy of the country
[12][28], despite its high nutritional value. The camel contribution to meat production started to increase not only in Egypt but also in other developing countries
[13][10], given the fact that camels are likely to have disease-resistance traits
[12][28]. Additionally, camels serve as a mode of transportation, particularly in the desert which is widely distributed in Egypt; therefore, they are an important component of nomadic life. Camel rearing is primarily practiced for recreational and entertainment purposes in tourist areas such as the Luxor and Red Sea governorates
[14][20]. In addition, camel racing is considered a popular traditional sport in many Arab countries, most notably in the Gulf region, and in Egypt, Bedouins of the South Sinai desert have kept up this tradition. To the Bedouins, the race is a way of keeping a traditional heritage alive. This race is considered an ancestral heritage and they are trying to preserve and renew it to hand it over from one generation to the next, which has been ongoing for at least the last 100 years
[15][29].
Smallholders occasionally raise camels in the countryside, together with other animals, or on their own farms. They can also do so in desert pastures like those in the Sinai Peninsula, the northwest coastal region, and the Red Sea coast
[16][18]. Between 2012 and 2015, Sudan and Ethiopia were the major sources of camels for Egypt, with more than 750,000 camel imports during this time
[6][17][19,30]. In fact, the Food and Agriculture Organization [FAO] recorded an increase in the camel population in Egypt from 111,000 in 2010 to about 149,500 in 2017
[12][28]. Notably, Egypt needs to import large numbers of live camels because the high rate of slaughtering is resulting in the fast depletion of the stock of available animals
[12][28].
2. Impact of Equine and Camel Piroplasmosis in Egypt
Since equines and camels are currently important resources for recreation and food production in Egypt, maintaining healthy populations of these species is critical. This diminishes the chances for the expansion of emerging zoonotic agents, such as Babesia microti and B. divergens, which may impact human health and create improved economic environments for the producers. In addition, uncontrolled camel piroplasmosis is also a threat to the production of critical food resources that can sustain the current high population growth rates in Egypt.
2.1. Equines
In rural areas of Egypt, the health and welfare of domestic equines are often neglected despite the high risk of contracting many infectious diseases, including African horse sickness, epizootic lymphangitis (EZL), rabies, trypanosomiasis, and piroplasmosis. Knowledge about the identification, management, and prevention of different infectious diseases is lacking in general
[18][31].
Equine piroplasmosis, recognized as one of the most frequent infectious tick-borne diseases (TBDs) in equids, is caused by the hemoprotozoan parasites
T. equi, B. caballi, and the newly identified species
T. haneyi [19][20][12,13]. It is possible, however, that additional and likely lowly virulent equine
Babesia and
Theileria species will be identified in the future. Infections with
T. equi and
B. caballi cause severe economic losses in the equine industry due to the cost of treatment, especially in acutely infected horses. Additionally, the absence of appropriate treatments can lead to the death of the animals
[5][6], and the infected and carrier equines are a common source of infection for ticks and other animals
[21][16].
Importantly, EP manifests as acute and persistent infections. Clinical signs are not specific to EP and vary from lacking to severe, whereas signs in acute cases are characterized by fever, anemia, hemoglobinuria, jaundice, edema, and even death
[22][32]. Furthermore, and because EP is also characterized by persistent infections, horses and donkeys may act as carriers for many years, particularly after
T. equi infection
[23][33]. It was found that
T. haneyi causes milder clinical disease (variable fever, anemia) than
T. equi in experimentally infected horses and is capable of superinfection with
T. equi [24][34]. After the acute phase of the disease, asymptomatic horses may continue to be infected and these asymptomatic horses may become reservoirs of infectious organisms for the appropriate vectors of ticks
[25][35]. Unfortunately,
T. haneyi does not appear to be susceptible to imidocarb diproprionate (ID), although most equine infections with U.S. strains of
T. equi can be treated with ID, and co-infections of horses with
T. equi and
T. haneyi reduce the effectiveness of ID against
T. equi. So, the global importance of
T. haneyi to equine health was recently shown through its resistance to ID and its interference with
T. equi clearance by ID in some co-infected horses
[24][34].
2.2. Camels
Although camels can tolerate harsh conditions, they can also be affected by climatic changes and by infections with different infectious diseases, including those caused by vector-borne hemopathogens, which frequently compromise the health and production of camels
[14][20].
Camel piroplasmosis (CP) is an acute to chronic infectious disease with a worldwide distribution that causes high morbidity and substantial economic losses
[16][18]. Similar to EP, CP can be caused by several
Theileria and
Babesia parasites, including
T. equi,
B. caballi,
B. bovis,
B. bigemina, among others
[26][17]. Clinical symptoms include anemia, hemoglobinuria, muscle trembling, and decreases in body temperature to a subnormal level a few hours of before death in untreated cases
[27][36].
Camel babesiosis, caused by several tick-borne
Babesia sp., is marked by severe morbidity and substantial economic loss
[28][15]. There is a lack of information about camel infections caused by
Babesia species, which are of zoonotic importance in Egypt. One of the most significant
Babesia species that affects humans is
Babesia microti, which may spread through blood transfusion or organ transplantation
[29][37]. Using molecular diagnostic methods and phylogenetic analysis of the discovered parasite, some researchers found
B. microti infections in camel breeds in Halayeb and Shalateen in Upper Egypt
[30][9]. This was a significant finding because the possible existence of camel reservoirs may represent a potential zoonotic risk to other animals and humans. In contrast to other animals, there is little knowledge of camels’ involvement in sustaining zoonotic tick-borne pathogens (TBPs), despite the importance of camels to human life in the country
[30][9].
3. Historical Overview of Equine and Camel Piroplasmosis in Egypt
3.1. Equine
Equine piroplasmosis has been currently reported in different geographic regions of Egypt (Assiut, Cairo, Giza, Qalubia, Kafr Elshiekh, Menofia, Alexandria, Ismailia, Faiyum, Al-Beheira, Matruh, and Beni Suef) (
Figure 1). In the past, the detection of the piroplasms in Egypt depended mainly on ME
[31][52]. After that, serological studies based on IFAT revealed exposure of equines to
T. equi [32][33][44,53] and
B. caballi parasites
[32][44] in the Cairo and Giza regions of Egypt. More sensitive serological methods, such as indirect (i) ELISA, also revealed the presence of
T. equi in horses and donkeys in Egypt
[32][34][35][44,45,54]. In addition, a competitive (c) ELISA based on the EMA-1 recombinant protein revealed the presence of
T. equi in horses and donkeys. However, a cELISA based on RAP-1 failed to detect
B. caballi in Egyptian equines in Cairo and Giza
[32][44], as well as in South Africa,
[36][55]. Possibly, given the sequence variability found among the
B. caballi RAP-1 proteins among distinct strains from different countries, it is possible that RAP-1-based serological methods, as currently designed, are not capable of effectively detecting
B. caballi infections worldwide.
Figure 1. Prevalence rate of EP in different geographical regions of Egypt according to the microscopic analysis (ME), serological examination (SE), and PCR. (1. Cairo, 2. Giza, 3. Qalubia, 4. Menofia, 5. Fayom, 6. Alexandria, 7. Assiut, 8. Kafr Elsheikh, and 9. Bani Suif).
Molecular techniques, such as PCR, have also recently been used to investigate the presence of
T. equi in horses in the country
[33][34][35][45,53,54]. Molecularly,
T. equi and
B. caballi were detected in horses and donkeys in Egypt
[32][37][7,44]. In addition,
T. haneyi was detected recently, for the first time, in horses and donkeys from Alexandria, Monufia, Ismailia, Giza, Faiyum, Beni Suef, and Cairo in Egypt
[37][7]. Combined serology and molecular results have shown that EP, caused by
T. equi,
B. caballi, and
T. haneyi, is widespread in several governorates of Egypt (
Table 12 and
Figure 1).
Altogether, the data collected using microscopic, serological, and molecular methods have revealed a wide prevalence of EP in Egypt (
Table 12 and
Figure 1)
[22][32][33][34][35][37][38][39][40][7,32,44,45,53,54,56,57,58]. The currently available data show that the incidence of
T. equi by microscopic analysis ranged between 11 and 38.9% in horses in Cairo and Giza. Moreover, in donkeys, EP ranged from 17.8 to 24.8% in Cairo and Giza.
Serological studies revealed that the incidence of
T. equi ranged from 23 to 50%, 17.9 to 30%, and 14.8 to 36.5% in horses using IFA, iELISA, and cELISA, respectively. Consistently, in donkeys, the serological prevalence of
T. equi was 31.4%, 53.4%, and 23.5–25.6% using IFA, iELISA, and cELISA, respectively.
Based on molecular techniques, the overall prevalence of
T. equi in horses ranged from 20 to 61.9%. and 13 to 50%. in donkeys. The prevalence of
B. caballi was 1.2–19.3% in horses and 0–15.7% in donkeys.
The recently identified
T. haneyi was also detected in Egypt, with an incidence of 53.1% in horses and 38.1% in donkeys
[37][7].
The wide range of variations in prevalence is shown in
Table 12, which may be due to the use of different diagnostic methods with different sensitivities and specificities and/or other differences among the sets analyzed, including different sample sizes and factors associated with the diversity existing among the distinct geographic areas studied. These observations highlight the fact that standardized and systematic surveys on EP have not been performed so far in Egypt. The serological prevalence of EP caused by three distinct agents (
T. equi,
B. caballi, and
T. haneyi) remains unknown. In addition, there are no commercially available or standardized enzymatic immunoassays based on crude, purified, or recombinant antigens derived from Egyptian strains of
T. equi,
B. caballi, or
T. haneyi for the rapid detection of chronically infected animals affected by EP using serological approaches.
Table 12.
The prevalence of EP in different governorates of Egypt using different diagnostic methods.
Figure 2. Prevalence rates of CP in different geographical regions of Egypt according to the ME, serological examination (SE), and PCR. 1. Cairo, 2. Giza, 3. Qalubia, 4. Sharkia, 5. Matruh, 6. Red sea, 7. Assiut, 8. Suhag, 9. Qena, 10. Luxur, and 11. Halayb w Shalaten.
Table 23.
The prevalence of CP in different regions of Egypt determined using microscopical and molecular techniques.
Method |
Year |
Governorates |
Sample Size |
Parasite |
Prevalence |
Reference |
Horses |
ME |
ME |
1992 | 2003 |
Different localities |
18 |
B. equi |
38.9% |
[ |
Cairo and Giza |
200 |
Theileria spp. |
30% |
[45][63] | 33][53] |
IFA |
50% |
ME |
1998 |
Cairo |
74 |
Theileria spp. |
33.3% |
[44][62 |
PCR |
77.8% |
] |
ME |
2011 |
Upper Egypt |
224 |
T. camelensis |
6.8% |
[43][61] |
Horses |
ME |
2011 |
Not detected |
100 |
T. equi |
18% |
[35] |
ME |
2014 | [ |
Assiut Upper Egypt |
89 | 54 | ] |
Babesia | spp. |
46.9% |
[ | 42 | ] | [60] |
Horses |
ME |
2013 |
Giza |
149 |
T. equi |
41.6% (Males 36.2% females 5.4%) |
[40][58] |
Theileria spp. |
9.1% |
Horses |
ELISA |
2015 |
Cairo and Giza |
50 |
ME |
2015 |
Giza |
243 |
Theileria spp. | T. equi |
22% 30% |
30.9% |
[46][64][38][56] |
Donkeys |
50 |
PCR |
10% |
Horses |
ME |
2016 |
Cairo and Giza |
139 |
Babesia spp. |
11.4% |
[34 |
ME |
2016 | ] | [ | 45 | ] |
Northern West Coastal zone |
331 |
Babesia | spp. |
11.9% |
[ | 13][10] |
Donkeys |
17.8% |
PCR |
B.bovis |
59.1% |
Horses |
IFA |
88 |
B. bigemina |
40.9% | T. equi |
23.9% |
Donkeys |
51 |
31.4% |
ME |
2018 |
Qalubia |
700 |
Babesia spp. Theileria spp. |
4.7% 0.4% |
[47][65] |
Horses |
cELISA |
88 |
T. equi |
14.8% |
PCR |
100 (negative ME) |
Babesia spp |
2% |
Donkeys |
51 |
23.5% |
nPCR |
2021 |
Halayeb and Shalaten |
142 |
B. bovis |
2.81% |
[16][18] |
Horses |
ME |
2016 |
Cairo and Giza |
168 |
ME |
2023 | T. equi |
27.4% |
[ | 34 |
Cairo, Giza, Qalubya, Sharika Suhag, and Red Sea |
531 |
Piroplasma spp. |
11% |
[21][26][16,17] | ][45] |
Donkeys |
cPCR | 133 |
24.8% |
Babesia/Theileria | spp. |
Horses |
nPCR |
168 |
T. equi |
61.9% |
Donkeys |
133 |
50.4% |
Horses |
cELISA |
168 |
T. equi |
15.5% |
38% |
Donkeys |
133 |
25.6% |
Horse |
iELISA |
168 |
T. equi |
17.9% |
Donkeys |
133 |
53.4% |
Horses |
ME |
2018 |
Cairo and Giza |
141 |
T. equi |
5.56% |
[39][57] |
Donkeys |
250 |
Mules |
5 |
Horses Donkeys Mules |
PCR |
45 |
T. equi |
30% |
50 |
5 |
Horses |
cELISA |
2020 |
Giza, Qalubia, Kafr, Elshiekh, and Menofia |
370 |
T. equi, |
39%, |
[22][32] |
B. caballi |
11% |
Donkeys |
150 |
T. equi, |
30.6% |
B. caballi, |
42% |
Horses |
mPCR |
2021 |
Alexandria, Monufia, Ismailia, Giza, Faiyum, Beni Suef, and Cairo. |
79 |
T. equi |
20.3% |
[37][7] |
B. caballi |
1.2% |
Mixed |
2.5% |
Donkeys |
76 |
T. equi |
13.1% |
B. caballi |
0 |
Mixed |
1.% |
Horse |
cPCR |
79 |
T. haneyi |
53.1% |
Donkeys |
76 |
T. haneyi |
38.1% |
Horses |
cPCR |
2022 |
AL-Faiyum, AL-Giza, Beni-Suef, Al-Menufia, Al-Beheira, and Matruh |
8 |
Piroplasma spp. |
0 |
[41][59] |
3.2. Camel
Camel piroplasmosis has been reported in different regions of Egypt, Cairo: Giza, and Assiut—upper Egypt; Qalubia-Halayeb and Shalaten—Northern West Coastal zone; Qena and Luxor—Sharika Suhag and the Red Sea (
Figure 2). First, the detection of CP was mainly dependent on ME
[42][43][44][45][60,61,62,63], which reported the infection of camels with
Theileria spp.,
T. camelensis, and
Babesia spp. with different infection rates, such as
Theileria spp. (9.1–33%),
T. camelensis (6.8%), and
Babesia spp. (46.9%). After that, a combination of ME and a molecular method (PCR) was used to obtain more accurate detection results
[13][26][46][47][10,17,64,65]. Combined microscopical and molecular results have shown that CP is caused by
Theileria spp.,
T. camelensis,
B. bovis,
B. bigemina,
T. annulate,
T. ovis,
T. equi,
B. caballi,
B. vulpes,
Babesia sp.
Theileria sp., and
B. microti, and it is widespread in several governorates of Egypt
[13][14][16][26][30][48][9,10,17,18,20,40] (
Table 23 and
Figure 2). It was found that camel can be infected with different
Piroplasma spp, suggesting infestations by different competent vectors. Overall, these data together suggest that camels should be screened for other species of
Babesia and
Theileria spp. that were not detected before via PCR using specific primer sets, followed by sequencing, in order to confirm the results.
mPCR |
T. equi |
(SI) |
41% |
T. equi |
(Mixed) |
0.5% |
B. caballi |
(Mixed) |
5.4% |
B. bovis (SI) |
4% |
B. bovis (Mixed) |
5% |
B. bigemmina (Mixed) |
0.5% |
nPCR |
B. vulpes |
22% |
Babesia sp. |
9% |
Theileria sp. |
3% |
nPCR |
2021 |
Halayb and Shalaten |
142 |
B. microti |
11.97% |
[30][9] |
PCR |
2022 |
Giza, Asyut, Sohag, Qena, Luxor, and the Red Sea |
148 |
B. bovis |
19.6% |
[14][20] |
B. bigemina |
14.9% |
Babesia sp. |
0.7% |
Theileria sp. |
1.4% |
T. equi |
0.7% |
nPCR |
2023 |
Cairo and Giza |
133 |
B. microti |
6.8% |
[48][40] |