Equine and Camel Piroplasmosis in Egypt: Comparison
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Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Heba Alzan.

Piroplasmosis is a global tick-borne disease caused by hemoprotozoan parasites, which causes high morbidity and substantial economic losses in farm animals. Equine and camel piroplasmosis causes significant losses worldwide and in Egypt. The multifactorial effects and overall impact of equine and camel piroplasmosis in Egypt remain poorly characterized.

  • equine
  • camel
  • piroplasma
  • Babesia
  • tick
  • tick borne diseases
  • Theileria
  • diagnosis

1. An Overview of tThe 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 [4,22][1][2].

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 [23][3].
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 [5,6][4][5].

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) [19,24,25,26][6][7][8][9]. 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 [8][10]. 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 [22,27][2][11]. 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) [28][12].
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 [28][12], despite its high nutritional value. The camel contribution to meat production started to increase not only in Egypt but also in other developing countries [10][13], given the fact that camels are likely to have disease-resistance traits [28][12]. 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 [20][14]. 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 [29][15].
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 [18][16]. 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 [19,30][6][17]. 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 [28][12]. 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 [28][12].

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 [31][18].
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 [12,13][19][20]. 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 [6][5], and the infected and carrier equines are a common source of infection for ticks and other animals [16][21].
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 [32][22]. 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 [33][23]. 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 [34][24]. 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 [35][25]. 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 [34][24].

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 [20][14].
Camel piroplasmosis (CP) is an acute to chronic infectious disease with a worldwide distribution that causes high morbidity and substantial economic losses [18][16]. Similar to EP, CP can be caused by several Theileria and Babesia parasites, including T. equi, B. caballi, B. bovis, B. bigemina, among others [17][26]. 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 [36][27].
Camel babesiosis, caused by several tick-borne Babesia sp., is marked by severe morbidity and substantial economic loss [15][28]. 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 [37][29]. 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 [9][30]. 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 [9][30].

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 [52][31]. After that, serological studies based on IFAT revealed exposure of equines to T. equi [44,53][32][33] and B. caballi parasites [44][32] 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 [44,45,54][32][34][35]. 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 [44][32], as well as in South Africa, [55][36]. 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.
Pathogens 12 01318 g001
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 [45,53,54][33][34][35]. Molecularly, T. equi and B. caballi were detected in horses and donkeys in Egypt [7,44][32][37]. 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 [7][37]. 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 21 and Figure 1). Altogether, the data collected using microscopic, serological, and molecular methods have revealed a wide prevalence of EP in Egypt (Table 21 and Figure 1) [7,32,44,45,53,54,56,57,58][22][32][33][34][35][37][38][39][40]. 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 [7][37]. The wide range of variations in prevalence is shown in Table 21, 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 21.
The prevalence of EP in different governorates of Egypt using different diagnostic methods.
Host Method Year Governorates Sample Size Parasite Prevalence Reference
Pathogens 12 01318 g002
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 32.
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 19922003 Different localities 18 B. equi 38.9% [ Cairo and Giza 200 Theileria spp. 30% [63][45]53][33]
IFA 50%
ME 1998 Cairo 74 Theileria spp. 33.3% [62][44 PCR 77.8%
]
ME 2011 Upper Egypt 224 T. camelensis 6.8% [61][43] Horses ME 2011 Not detected 100 T. equi 18% [54]
ME 2014[ Assiut

Upper Egypt		 8935]
Babesia spp. 46.9% [60][42] Horses ME 2013 Giza 149 T. equi 41.6% (Males 36.2% females 5.4%) [58][40]
Theileria spp. 9.1% Horses ELISA 2015 Cairo and Giza 50
ME 2015 Giza 243 Theileria spp.T. equi 22%

30%		 30.9% [64][46][56][38]
Donkeys 50
PCR 10% Horses ME 2016 Cairo and Giza 139 Babesia spp. 11.4% [45
ME 2016][34]
Northern West Coastal zone 331 Babesia spp. 11.9% [10][13] 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%		 [65][47] 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% [18][16] Horses ME 2016 Cairo and Giza 168
ME 2023T. equi 27.4% [45 Cairo, Giza, Qalubya, Sharika Suhag, and Red Sea 531 Piroplasma spp. 11% [16,17][21][26]][34]
Donkeys
cPCR133 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% [57][39]
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%, [32][22]
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% [7][37]
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 [59][41]

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 [60[42][43][44][45],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 [10,17,64,65][13][26][46][47]. 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 [9,10,17,18,20,40][13][14][16][26][30][48] (Table 32 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% [9][30]
PCR 2022 Giza, Asyut, Sohag, Qena, Luxor, and the Red Sea 148 B. bovis 19.6% [20][14]
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% [40][48]
SI: single infection.

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