Molecular Epidemiology and Species Diversity of Tick-Borne Pathogens: History
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Ticks and tick-borne pathogens (TTBPs) are listed among the most serious concerns harming Egyptian livestock’s productivity. Several reports on tick-borne pathogens (TBPs) from various geographical regions in the country were published. There is evidence of high species diversity of the TBPs infecting animals from Egypt, which suggests endemicity and complex transmissions. Animals from Egypt and their infesting ticks were found to harbor many zoonotic and/or potentially zoonotic pathogens, such as A. phagocytophilum (anaplasmosis), B. microti and B. divergens (babesiosis), Borrelia burgdorferi (Lyme disease), Coxiella burnetii (Q fever), rickettsiosis, CCHFV (Crimean–Congo hemorrhagic fever), and Ehrlichia spp. (ehrlichiosis), which can be transmitted to their accompanying farmers. Ticks that infest animals and their associated pathogens displayed high species diversity, underlining the high infection risk to animals as well as constituting a reservoir for a wide range of zoonotic TBPs. Adequate control measures against TTBPs should be applied to prevent their circulation among animals in the country.

  • tick-borne diseases
  • Egypt
  • molecular
  • Anaplasma
  • Babesia
  • Theileria

1. Introduction

Tick-borne diseases (TBD) are important factors that constrain the development of livestock industries worldwide and can cause losses estimated to be billions of dollars for farmers annually [1,2]. Phenotypic traits are proven to have limited taxonomic significance in identification and delimitation of various species during microscopical examination [3,4]. The use of molecular diagnostic tools in studying tick-borne agents has increased in recent decades because of its high sensitivity and accuracy [5,6,7,8]. With the advancement of molecular biology, new species, strains, or genetic variants of microorganisms are being discovered in ticks all over the world, and the list of potential tick-borne infections is growing [9].
Egypt’s population is rapidly growing. The estimated population in 2020 was 102.3 million with an annual rate of population change of 2.03% (United Nations population estimates and projections; (accessed on 1 June 2022). The local animal population exceeded 18 million, comprising 5.1 million cattle, 3.7 million water buffaloes, 5.4 million sheep, 4 million goats, 120,000 camels, and 85,000 horses [10,11]. Food security is one of the challenges facing the world due to the fast-rising human population, and the global prevalence of undernourished people increased drastically between 2019 and 2020, owing primarily to the COVID-19 pandemic [12]. Stakeholders were urged to adopt a One Health approach to designing and implementing livestock policies and investments, particularly in dealing with emerging and re-emerging animal diseases that, if left uncontrolled, could endanger the development trajectory of the entire livestock sector [10].

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 our 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, we 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 [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 [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 [1,40].

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 we 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 [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 [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 [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 [44,45,46]. Furthermore, molecular and serological data show that Q fever may play a role in sheep and goat abortions [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 [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 [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 [54]. The zoogeographical range of ticks and the diseases they transmit are limited by host movements and climatic variables [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%) [57]. Egypt obtains camels from Sudan, Somalia, Ethiopia, Eritrea, and Kenya by way of Ethiopia [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 [60]. Babesia canis has been further categorized into three subspecies (B. canis, Babesia canis rossi, and B. canis vogeli) [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 [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 our 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 [63]. Ticks tend to be general global hosts but specialist local hosts [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 [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 [67,68].

This entry is adapted from the peer-reviewed paper 10.3390/pathogens11080912

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