2. TBPs in Cattle and Buffaloes in Egypt
Five of the thirty-seven molecular studies on bovines were not used for meta-analysis; the included data on those five were distinguished between cattle and buffaloes, or the number of positives was not clearly specified. Therefore, 32 studies were included, comprising 23 studies on cattle only, 1 study on buffaloes only, and 8 studies on both cattle and buffaloes. These studies molecularly tested 7213 cattle and 626 buffaloes for various TBPs
(Table S1).
In total, 14 data sets describing
Babesia infections in 3203 cattle were revealed during
theour database search, and 525 cases were found to be infected, resulting in a pooled prevalence of 16.0% (95% CI, 10.9–21.0%). Two
Babesia spp. were frequently detected and displayed similar prevalences:
Babesia bigemina (10.1%, CI, 6.3–13.8%) and
Babesia bovis (9.5%, CI, 6.0–13.0%). A few datasets detected other species, e.g.,
Babesia ovis (7.3%) and
Babesia occultans (0.3%).
Theileria infections were the most frequently tested TBPs in cattle; 17 data sets tested 4620 cattle, and 1324 were found to be infected, giving rise to a pooled global prevalence of 36.0% (95% CI, 23.4–48.7%). Of the species detected,
T. annulata was the predominant (30.8%), whereas a much lower prevalence was estimated for
Theileria orientalis (3.0%). For
Anaplasma infections,
rwe
searchers collected 9 data sets that tested 1745 cattle, and 510 animals were found to be infected, resulting in the highest pooled prevalence (43.9%, CI, 4.8–83.1%) among TBPs infecting cattle. Likewise,
Anaplasma displayed the greatest species diversity among cattle TBPs; several
Anaplasma species were identified, including
Anaplasma marginale (21.2%),
Anaplasma centrale (1.4%),
Anaplasma platys-like (8.3%),
Anaplasma platys (8.4%),
Anaplasma phagocytophilum (15.0%), and
Anaplasma ovis (3.4%). It is noteworthy that in 2020 and 2021,
Anaplasma infections outnumbered
Babesia and
Theileria infections in many cattle farms in Egypt (personal communication with various field veterinarians). However, the prevalence of the variations among the three common TBPs (
Babesia,
Theileria, and
Anaplasma) infecting cattle were statistically insignificant (
p value = 0.1960). Other miscellaneous TBPs that infect cattle were detected in lower prevalences, including
Bartonella spp. (2.6%),
Borrelia spp. (2.9%),
Coxiella burnetti (7.2%), and
Rickettsia sp. (1.1%).
Although the population of water buffaloes in Egypt is not much different than that of cattle, buffaloes have received little attention concerning TBPs. Similar to the TBPs in cattle,
Anaplasma species were the most prevalent TBPs in buffaloes with a pooled prevalence of 26.9% (95% CI, 7.3–61.1%), and
A. marginale,
A. platys-like, and
A. platys were the identified species. The other TBPs detected in buffaloes displayed minor prevalences, e.g.,
Babesia species (
B. bigemina and
B. bovis) had a pooled prevalence of 3.6% (95% CI, 0.6–6.6%). Many field veterinarians in Egypt rely on combined conjunctivitis–lymphadenopathy as a specific symptom to diagnose chronic theileriosis in buffaloes. Based on personal communications, the disease is common in Egypt particularly during summer in 2020 or 2021. However, the estimated pooled prevalence for
Theileria infections in buffaloes did not exceed 1.0%. A possible explanation for this very low prevalence in comparison to cattle (36.0%) is the limited number of tested buffaloes (247). It is noteworthy that many other pathogens can cause eye infections in buffaloes, particularly
Moraxella bovis, which may lead to disease misdiagnosis. The low detection rate of piroplasms in water buffaloes may be attributed to their wallowing in muddy waters to maintain their body temperature, together with their thick hide, which contributes to lower tick attachment
[13][14][15][34,35,36].
Bartonella species were also detected in buffaloes and expressed a higher prevalence (5.0%) than they did in cattle (2.6%).
Anaplasmosis (primarily caused by
A. marginale and
A. centrale), babesiosis (
B. bovis,
B. bigemina, and
Babesia divergens), and theileriosis (
T. annulata,
Theileria parva, and
T. orientalis complex) affect bovines worldwide, causing significant economic losses to the cattle industry, especially in the tropics and subtropics
[16][17][18][37,38,39]. Thus, the frequent detection of these parasites from bovines in Egypt is alarming and requires the establishment of effective surveillance and control strategies.
Anaplasma marginale is the most prevalent among TBPs in buffaloes (37.5%) and the second most prevalent in cattle (21.2%) in Egypt (after
T. annulata). This parasite is also the most prevalent tick-borne pathogen globally in bovines, causing a mild to severe hemolytic disease with considerable economic loss
[1][19][1,40].
3. TBPs in Sheep and Goats in Egypt
TBPs are not popular among small ruminant producers in Egypt, most likely due to the restricted resultant economic loss, in comparison with the various viral and bacterial diseases that are highly prevalent in sheep in Egypt. Fourteen studies were found that detailed the prevalence of TBPs in 1286 sheep and 263 goats
(Table S2), and
rwe
searcher included 6 data sets that described
Babesia and
Theileria infections in sheep with estimated pooled prevalences of 3.8% and 11.0%, respectively.
Anaplasma infections were also the most prevalent (16.1%, CI, 6.6–23.5%) in sheep and were investigated in four data sets, encompassing 599 animals. Other TBPs detected in sheep have displayed variable prevalences:
Bartonella spp. (3.1%, CI, 3.3–9.6%),
Borrelia spp. (3.4%, CI, 1.2–8.1%), and
Rickettsia spp. (13.7%, CI, 12.1–39.6%). Notably, six data sets described
C. burnetti infections in 309 sheep, and 94 animals were found positive, giving rise to a very high estimated pooled prevalence (45.3%, CI, 9.5–81.2%). Moreover, a diverse fauna of TBPs were identified in sheep, including various species of the genus
Babesia (
B. bovis,
B. bigemina, and
B. ovis), the genus
Theileria (
T. annulata,
Theileria ovis, and
Theileria lestoquardi), and the genus
Anaplasma (
A. marginale,
A. ovis,
A. phagocytophilum,
A. platys, and
A. platys-like).
Babesia ovis and
T. lestoquardi are the most pathogenic tick-borne haemoparasites in small ruminants worldwide
[20][41].
Meanwhile, the data on TBPs in goats in Egypt are less informative since very few data sets (
n = 4) were found. Four TBPs were investigated, including
Theileria (50.0%),
C. burnetti (29.4%),
Babesia (16.7%), and
Bartonella (2.0%). Q fever is a globally transmitted zoonotic infection caused by the intracellular Gram-negative bacterium
C. burnetii [21][42]. Excretion of
C. burnetii in tick faeces and saliva is widely reported, and the prevalence of
C. burnetii in ticks from various bioclimatic zones and socioeconomic contexts suggests their potential role in the epidemiology of Q fever
[22][43]. Although the molecular data indicated a high prevalence of Q fever in sheep and goats in Egypt, some of examined samples were seropositive and/or from aborted animals. While the high prevalence of
C. burnetti is suggestive of the potential role of sheep and goats in the transmission of Q fever to people in Egypt, serosurveys from humans in Egypt are scarce
[23][24][25][44,45,46]. Furthermore, molecular and serological data show that Q fever may play a role in sheep and goat abortions
[24][26][27][45,47,48].
4. TBPs in Equines in Egypt
Nine studies that tested 855 horses and 546 donkeys were used in the meta-analyses conducted to estimate the pooled prevalence for various TBPs infecting equines in Egypt
(Table S3).
Theileria spp. were most prevalent in horses (34.1%, 95% CI, 12.9–55.3%) and donkeys (30.6%, 95% CI, 14.0–47.2%).
Theileria equi and
Theileria haneyi were identified in both horses and donkeys. Moreover,
Theileria sp. Africa were detected in horses, whereas
T. ovis were found in donkeys. Two data sets described Babesiosis (
Babesia caballi) in horses and donkeys, with pooled prevalences of 9.8% (CI,−7.8–27.5%) and 7.2% (CI,−7.2–21.5%), respectively.
Bartonella spp. were also identified in horses (0.8%) and donkeys (5.1%); meanwhile, infection with
Anaplasma spp. (
A. marginale and
A. ovis) was detected only in donkeys (26.7%). Equine piroplasmosis is an important tick-borne disease caused by the hemoprotozoan parasites
T. equi and
B. caballi, resulting in major economic losses to the equine industry
[28][29][30][49,50,51].
5. TBPs in Dromedary Camels in Egypt
The dromedary (
Camelus dromedarius), also referred to as the Arabian camel, dromedary camel, or one-humped camel, is a large even-toed ungulate that belongs to the family Camelus. In the Old World region, the domesticated dromedary is typically found in semi-arid to arid areas, primarily in Africa and the Arabian Peninsula, though there is also a sizable feral population in Australia
[31][32][52,53].
Camels can host a wide range of very diverse TBPs. However, a few studies (
n = 11) on dromedaries in Egypt that tested 1268 animals were found during the database search and determined to be suitable for the meta-analysis
(Table S4). In general, high TBPs’ prevalence was detected, regardless of the limited number of datasets. Various species of
Babesia (11.0%),
Theileria (71.8%), and
Anaplasmsa (40.5%) as well as C.
burnetti (20.8%) and
Rickettsia spp. (31.9%) were identified in the tested dromedaries in Egypt. Of note, the TBPs detected in camels were more highly diverse than those of any other animal species. The zoonotic species
Babesia microti was interestingly identified in the blood of 17 out of 142 camels in one study.
Babesia microti infects humans and is considered to be an important transfusion-transmitted infectious agent. Between 2010 and 2014, the parasite caused 4 out of 15 deaths associated with transfusion-transmitted infections in the United States
[33][54]. The zoogeographical range of ticks and the diseases they transmit are limited by host movements and climatic variables
[34][35][55,56]. In Egypt, significant numbers of animals are imported to compensate the gap in the livestock industry. All imported cattle are slaughtered in quarantine stations’ facilities. Camels are imported from various countries in East Africa and may be transferred to slaughterhouses or to various animal markets after being released from the quarantine. The Birqash market near Cairo is Africa’s biggest camel market. Between 2012 and 2015, a total of 762,291 camels were legally imported into Egypt from Sudan (79.4%) and Ethiopia (20.6%)
[36][57]. Egypt obtains camels from Sudan, Somalia, Ethiopia, Eritrea, and Kenya by way of Ethiopia
[37][38][58,59]. Consequently, camel transportation could explain the more highly diverse fauna of TBPs in camels than that of all other animal hosts in Egypt.
6. TBPs in Dogs in Egypt
The majority of the dogs in Egypt are strays. Recently, owning a dog became popular among youth in many urbanized areas. Nonetheless, data on TBPs in dogs from Egypt are scarce. Ten studies that tested 1950 dogs for TBPs were included in the meta-analysis. The most prevalent TBPs in dogs was
Babesia spp.; 105 out of 924 tested dogs were found to be infected, with a pooled prevalence of 22.8% (CI, 13.0–32.7%). The reports named the species present as
Babesia vogeli and
Babesia canis. However, the sequenced isolates were completely identical, suggesting that all isolates belonged to the same species,
Babesia canis vogeli.
Babesia canis and
Babesia gibsoni are the two species that are responsible for most canine babesiosis cases worldwide
[39][60].
Babesia canis has been further categorized into three subspecies (
B. canis,
Babesia canis rossi, and
B. canis vogeli)
[40][61]. Other tick-borne infections were detected in lower prevalences in dogs from Egypt, such as anaplasmosis (3.5%), ehrlichiosis (5.7%), rickettsioses (1.5%), and borreliosis (0.8%).
7. Tick-Associated Pathogens in Egypt
Egypt has a warm climate, and the temperature often does not drop below 15 °C in the cold months (December–February). Therefore, high tick activity can occur throughout the year. Even in cold months, aggregates of ticks can be noticed on animals. Tick control is an important strategy for combating TBPs that infect animals. In Egypt, a weekly application of acaricides is used by many cattle farms to control ticks, and prolonged incorrect use of the acaricides could result in the development of acaricide-resistant tick populations, reducing the number of effective acaricides in the market and creating a potential future problem for controlling TBPs
[41][62]. Ticks and/or tick pools from 17 studies were combined for estimating the pooled prevalence of various TBPs, and an analysis was conducted in relation to the identified tick genera. In
theour analysis, ticks belonging to the genus
Boophilus were moved to the genus
Rhipicephalus. In the included studies, three genera of Ixodid ticks (
Rhipicephalus,
Hyalomma, and
Amblyomma) were identified and molecularly investigated for their harbored pathogens. Notably,
Theileria infections were identified in tested ticks from ineligible studies for meta-analysis
(Table S6). However, ticks of the genus
Rhipicephalus (the most frequently tested in 22 datasets) were infected with various
Babesia (
B. bovis and
B. bigemina) and
Anaplasma (
A. marginale,
A. platys,
A. platys-like, and
A. phagocytophilum) species.
Borrelia spp.,
Rickettsia spp., and
C. burnetti were identified with variable prevalences in the three tested tick genera. The pooled prevalence variability and diversity of TBPs in tested ticks was mainly attributed to the use of specific oligonucleotide primers and probes to detect several species of TBPs. Two datasets tested 1248 ticks collected from camels of the genus
Hyalomma (
H. dromedarii and
H. rufipes) and found the Crimean–Congo hemorrhagic fever virus (CCHFV) in 18 (1.4%). Similarly, the same tick species (six pools) that infested camels were found to be positive for CCHFV among the 138 tick pools collected from different animals
(Table S6). While the camels that tested positive were imported to Egypt, no reports included this virus in the testing conducted on animals from Egypt. Of note, a study that investigated soft ticks of the genus
Ornithodoros (
O. savignyi) detected a high prevalence (66.0%) of
Borrelia burgdorferi.
Since vertebrate reservoir competence for different pathogens varies widely among species, vector host specificity is critical for understanding the epidemiology of tick-borne infections
[42][63]. Ticks tend to be general global hosts but specialist local hosts
[42][43][63,64]. Taking into consideration the close interactions of diverse animal species (e.g., sheep and goats), the presence of mixed animal shelters, and the unregulated animal movements in Egypt, the likelihood of a pathogen crossing a species barrier is increased
[44][45][65,66]. Circulations of some TBPs in Egypt among various ruminants were evident, e.g.,
T. annulata,
B. bigemina,
B. bovis, and
A. marginale. Multiple pathogen co-infections have an impact on tick vector colonization and transmission to vertebrate hosts, and they can be generated either by ticks feeding on the blood of a variety of vertebrate hosts or by co-feeding
[46][47][67,68].