This is the first comprehensive study of Hyalomma ticks attached to domestic animals and their associated Anaplasma/Ehrlichia species conducted on the border of Iran and Pakistan, southeast corner of Iran. The results show that there are six infesting Hyalomma spp., ticks and that there are at least three Anaplasmosis agents that can be transmitted through a tick bite.
These infestations may cause considerable blood losses from livestock and can also transmit severe tick-borne diseases in the region. These diseases impose massive losses on the livestock sector including reducing the production of meat, milk, wool, and skin in the south corner of Iran. Results of this study is generally in accordance with observations on hard ticks and pathogens from animals in Pakistan neighbouring country and other parts of Iran, while there are some distinctive results in this study [7, 17, 22].
In this study, Hy. anatolicum-infested animals were found to be the most common and have the widest geographical range. This three-host tick species was previously reported as the most prevalent hard tick from different parts of Pakistan including Baluchistan of Pakistan the closest area to Baluchistan of Iran, and most parts of Iran [7, 8, 17, 18, 19, 20].
The present study provides new information about the risks of high diverse Hyalomma infestation of domestic animals in south-eastern Iran. This situation may address the animal traffic from neighbouring countries, which may lead to more frequent encounters with these tick species. The ticks in this study were feeding on the animals at the time of collection and were, therefore, potentially transmitting any Anaplasma spp., to the animals while feeding. However, the possibility that these ticks play a significant role in Anaplasmosis transmission to domestic animals where it is endemic requires further investigation. Hyalomma spp., ticks in this region carried the Anaplasma and Ehrlichia agents, including A. ovis, A. marginale, and E. ewingii. These Anaplasmataceae pathogens were previously detected using molecular methods in hard ticks in several regions in Iran [17, 19, 20, 21]. The prevalence of Hyalomma spp., with Ehrlichia /Anaplasma spp., DNA in this study was 68%, which is higher than the rate of infection in the previous reports from other parts of the country. The prevalence of infection was reported as 4.6% [17], 25% [22], 43.84% [23], and 55.5% [9]. The different results regarding the tick infection rate in the study region could be explained by the different environmental factors, collection time, the sampling method, the tick community structure.
The result of this study and the above literature showed that different species of Hyamlomma could be one of the primary carriers and reservoirs for Anaplasma /Ehrlichia spp., in the country. In addition to Hyalomma spp., ticks, other hard ticks including Rhipicephalous bursa, R. sanguineous, Dermacentor marginaus, Haemaphysalis erinacei, Ixodes ricinus [7, 8, 17, 23] are reported as vectors of different tick-borne bacteria of the family Anaplasmataceae. However, in other parts of the world, the most important vector of anaplasmosis belongs to different species of Ixodes genus; for example, Ixodes ricinus in Europe, I. persulatus in Eastern Europe and Asia, and I. scapularis in North America [24].
In this study a high prevalence of the anaplasmataceae species (81.82%) was of A. ovis DNA. This bacterium was isolated from five tick species of Hy. anatolicum (31.8%), Hy. asiaticum (13.6%), Hy. marginatum (18.2%), Hy. dromedarii (0.9%), and Hy. detricum (0.9%) which were collected from cattle, goat, and camel. Anaplasma marginale and E. ewingii were found only from Hy. schulzi and Hy. dromedarii collected on goats and camels respectively. Both A. ovis and A. marginale are important livestock pathogens whereas E. ewingii is an important human pathogen. Ehrlichia ewingii mainly infects granulocytes, triggering granulocytic Ehrlichiosis in dog and human [4, 34]. Granulocytic Ehrlichiosis in humans has been described in immunosuppressed as well as immunocompetent patients, causing headache, fever, myalgia, vomiting, nausea, acute renal failure, thrombocytopenia, leukopenia and increased liver enzyme activities [25–27]. Anaplasma ovis is less pathogenic than other Anaplasma species, has got worldwide distribution, and is responsible mostly for small ruminant anaplasmosis with a low ranking fever [28, 29]. However, it may be an important disease agent for sheep and goat [30, 31]. Fever, anorexia, fatigue, milk reduction and abortion with a low death rate are the common clinical marks of A. ovis in infected animals [32]. Anaplasma marginale is known as the most important rickettsia disease in cattle. The common clinical signs of the disease are progressive haemolytic anaemia, decrease milk production, abortions, and death. In addition to cattle, other animals including water buffalo, and wild mammals like deer can be infected [33].
The present study revealed circulation of three species of Anaplasmatacea along the border of Iran and Pakistan. This finding is in agreement with the results of researchers on the border of Iran and Afghanistan as well as Pakistan who reported different tick-borne pathogens including Ehrlichia and Anaplasma in ticks [8, 18]. In Pakistan, researchers reported A. marginale, A. centrale, A. ovis, A. platys-like organism, E. minasensis, and two uncharacterized species: Ehrlichia sp., Multan and Anaplasma spp., (BL099-6).
In the current study we did not find A. phagocytophilum or other human granulocytic ehrlichiosis (HGE) agent in the tick specimens. Using more sensitive methods such as real-time PCR (RT-PCR) against ticks or the animal blood of tick hosts might reveal better picture of anaplasmosis agent in the region. Anaplasma phagocytophilum can infect various animals including goats and cows, and can be transmitted to humans by a bite from an infected tick [4].