Using genomic approaches to unravel livestock (host)-tick-pathogen interactions

Ticks and tick-borne diseases are a major constraint on livestock farming in many developing countries, which has a huge impact on their economies. Genomic information is becoming more abundant for many of the species involved, which if exploited successfully could be used to develop new control strategies. Here, we review the genomic resources that are now available and discuss how this information is currently being harnessed or can be used in the future to explore the complex interplay that occurs between livestock hosts, tick vectors and tick-borne pathogens.     

Abiotic and biotic determinants of tick burdens in the eastern rock sengi (Elephantulus myurus)

Ticks are important vectors of pathogens of medical and veterinary importance worldwide. In spite of their economic importance, our current knowledge about the factors affecting tick prevalence and abundance in tropical and subtropical regions is rather limited. Both abiotic (e.g. temperature) as well as biotic variables (e.g. host sex) have been identified as key determinants of distributions. Eastern rock sengis or elephant shrews (Elephantulus myurus, Macroscelidea: Cacroscelididae, Thomas & Schwann) are widely distributed throughout Africa and can harbour a large number of tick species and substantial tick burdens. In the present study, we evaluated the contribution of climate and host factors on tick burdens of sengis. Throughout the year sengis carried high abundances of immature stages of a single tick species, Rhipicephalus sp. near warburtoni. There was no evidence that host parameters affected tick burdens. However, larval abundance decreased with increasing ambient temperatures and both larvae and nymphs were negatively affected by rainfall 2 months before the sampling month. In addition, nymphal burdens decreased with increasing minimum temperatures. Our results suggest that climate factors are the largest constraint for the immature stages of R. sp. near warburtoni and that eastern rock sengis could play a crucial role in the dynamics of tick-borne diseases as a result of the large tick burdens they can sustain.     

Detection of Anaplasma bovis in an undescribed tick species collected from the eastern rock sengi Elephantulus myurus

Ticks are important vectors of numerous pathogens causing illness, fatalities, and economic loss worldwide. Infectious disease episodes are increasing, and novel tick-borne pathogens are described frequently. Identification of novel reservoir hosts and vectors of tick-borne pathogens is essential if control measures are to be successful. In South Africa, the eastern rock sengi, Elephantulus myurus , hosts a number of tick species of veterinary importance. Despite this, there remains a paucity of information regarding the tick fauna of this species, the pathogen associations of ticks that it hosts, and its role as a reservoir host of tick-borne pathogens. The current study documents the tick fauna of E. myurus and sympatric small mammal species in Limpopo Province, South Africa. The pathogen associations of ticks hosted by elephant shrews were also investigated by PCR screening of engorged nymphs for a broad range of bacterial and protozoan tick-borne infections, including Borrelia burgdorferi sensu lato and members of Apicomplexa and the order Rickettsiales. There were marked differences in tick species and abundance among host species. Elephantulus myurus was heavily, and predominantly, parasitized by an as-yet undescribed tick species that we identify as Rhipicephalus sp. near warburtoni. PCR and sequence analysis revealed the presence of Anaplasma bovis in this tick species, which may have consequences for livestock production and conservation efforts in the area where this tick species occurs.     

Tick-borne haemoparasitic diseases in small ruminants in Pakistan: Current knowledge and future perspectives

Livestock industry is an essential part of Pakistan’s economy, and a variety of ruminants (including sheep and goats) are reared for the increasing demand of milk, meat and hide products. Haemoparasitic illnesses such as theileriosis, anaplasmosis, and babesiosis are a significant health risk for small ruminants in our country. Information regarding distribution patterns, the tick species involved and effective strategies to control tick-borne diseases (TBD) in goats and sheep of Pakistan is limited. To this end, it is required to assess the present rank of TBDs in small ruminants of Pakistan with a note on their vector ticks in order to control and identify the gaps in the knowledge of TBDs. This will recommend areas for future research and will add to the understanding of these diseases and will draw attention to the need for better-quality tools for the diagnosis and control of TBDs in small ruminants of Pakistan.     

Biodiversity in the Lyme-light: ecological restoration and tick-borne diseases in Europe

Biodiversity loss and the emergence of zoonotic diseases are two major global challenges. An urgent question is how ecosystems and wildlife communities can be restored whilst minimizing the risk of zoonotic diseases carried by wildlife. Here, we evaluate how current ambitions to restore Europe’s natural ecosystems may affect the hazard of diseases vectored by the tick Ixodes ricinus at different scales. We find that effects of restoration efforts on tick abundance are relatively straightforward but that the interacting effects of vertebrate diversity and abundance on pathogen transmission are insufficiently known. Long-term integrated surveillance of wildlife communities, ticks, and their pathogens is needed to understand their interactions and to prevent nature restoration from increasing tick-borne disease (TBD) hazard.     

Projecting the potential distribution of ticks in China under climate and land use change

Ticks are known as vectors of several pathogens causing various human and animal diseases including Lyme borreliosis, tick-borne encephalitis, and Crimean-Congo hemorrhagic fever. While China is known to have more than 100 tick species well distributed over the country, our knowledge on the likely distribution of ticks in the future remains very limited, which hinders the prevention and control of the risk of tick-borne diseases. In this study, we selected four representative tick species which have different regional distribution foci in mainland China. i.e., Dermacentor marginatus, Dermacentor silvarum, Haemaphysalis longicornis and Ixodes granulatus. We used the MaxEnt model to identify the key environmental factors of tick occurrence and map their potential distributions in 2050 under four combined climate and socioeconomic scenarios (i.e., SSP1-RCP2.6, SSP2-RCP4.5, SSP3-RCP7.0 and SSP5-RCP8.5). We found that the extent of the urban fabric, cropland and forest, temperature annual range and precipitation of the driest month were the main determinants of the potential distributions of the four tick species. Under the combined scenarios, with climate warming, the potential distributions of ticks shifted to further north in China. Due to a decrease in the extent of forest, the distribution probability of ticks declined in central and southern China. In contrast with previous findings on an estimated amplification of tick distribution probability under the extreme emission scenario (RCP8.5), our studies projected an overall reduction in the distribution probability under RCP8.5, owing to an expected effect of land use. Our results could provide new data to help identify the emerging risk areas, with amplifying suitability for tick occurrence, for the prevention and control of tick-borne zoonoses in mainland China. Future directions are suggested towards improved quantity and quality of the tick occurrence database, comprehensiveness of factors and integration of different modelling approaches, and capability to model pathogen spillover at the human-tick interface.     

Historical review and insights on the livestock tick-borne disease research of a developing country: The Philippine scenario

Tick-borne diseases (TBDs) remain to be a global animal health threat. Developing countries like the Philippines is not exempt to this. Despite the potential impact TBDs can give to these countries, local government initiatives and researches remain to be limited. In the Philippines, most epidemiological studies were confined only to specific areas, and predominantly in the Northern Area. Due to its unique geography and limited studies, the current nationwide status of most TBDs could not be clearly established. This review mainly covered published studies and presented challenges in the conduct of TBD research in the Philippines, which may be similar to other Southeast Asian or developing countries. To date, reported livestock TBD pathogens in the Philippines include Anaplasma, Babesia, Theileria, and Mycoplasma spp. With the ubiquitous presence of the Rhipicephalus microplus ticks in the country, it is highly probable that other pathogens transmitted by these vectors could be present. Despite studies on different TBDs in the livestock sector, the Philippine government has not yet heightened its efforts to implement tick control measures as part of the routine animal health program for local farmers. Further studies might be needed to determine the nationwide prevalence of TBDs and the presence of other possible tick species and TBD pathogens. The Philippine scenario may present situations that are similar to other developing countries.     

Tick-Borne Viruses

Ticks are important vectors for the transmission of pathogens including viruses. The viruses carried by ticks also known as tick-borne viruses (TBVs), contain a large group of viruses with diverse genetic properties and are concluded in two orders, nine families, and at least 12 genera. Some members of the TBVs are notorious agents causing severe diseases with high mortality rates in humans and livestock, while some others may pose risks to public health that are still unclear to us. Herein, we review the current knowledge of TBVs with emphases on the history of virus isolation and identification, tick vectors, and potential pathogenicity to humans and animals, including assigned species as well as the recently discovered and unassigned species. All these will promote our understanding of the diversity of TBVs, and will facilitate the further investigation of TBVs in association with both ticks and vertebrate hosts.     

Tick salivary secretion as a source of antihemostatics

Ticks are mostly obligatory blood feeding ectoparasites that have an impact on human and animal health. In addition to direct damage due to feeding, some tick species serve as the vectors for the causative agents of several diseases, such as the spirochetes of the genus Borrelia causing Lyme disease, the virus of tick-borne encephalitis, various Rickettsial pathogens or even protozoan parasites like Babesia spp. Hard ticks are unique among bloodfeeders because of their prolonged feeding period that may last up to two weeks. During such a long period of blood uptake, the host develops a wide range of mechanisms to prevent blood loss. The arthropod ectoparasite, in turn, secretes saliva in the sites of bite that assists blood feeding. Indeed, tick saliva represents a rich source of proteins with potent pharmacologic action that target different mechanisms of coagulation, platelet aggregation and vasoconstriction. Tick adaptation to their vertebrate hosts led to the inclusion of a powerful protein armamentarium in their salivary secretion that has been investigated by high-throughput methods. The resulting knowledge can be exploited for the isolation of novel antihemostatic agents. Here we review the tick salivary antihemostatics and their characterized functions at the molecular and cellular levels.     

Present status of tick-borne diseases in Sudan

Ticks and tick-borne diseases are widespread in the Sudan, cause substantial economic losses and constitute major obstacles to the development of animal wealth. Most important among these diseases are tropical theileriosis, malignant ovine theileriosis, cowdriosis, babesiosis, anaplasmosis and avian spirochaetosis. However, knowledge about ticks and tick-borne diseases is still fragmentary and far from complete. The large number of tick species, the multplicity of transmitted agents and the diverse ecoclimatic zones of the Sudan provide a unique opportunity to host diverse research activities that could benefit other regions in Africa.     

Use of DNA sequences for Rickettsia identification in Ixodes ricinus ticks: the first detection of Rickettsia monacensis in Poland

The cosmopolitan tick Ixodes ricinus inhabiting Europe, including Poland, is a vector for many pathogens, such as various Rickettsia species, which spread to new territories. They are present mainly in the Mediterranean countries, but have also been found in Central Europe at increasing frequency. In the present study, the gltA gene, encoding citrate synthase, and an internal transcribed spacer (ITS) were employed to detect the DNA and identify the species of tick-borne pathogens of the Rickettsia genus. The presence of bacterial DNA was detected in 9.5% of the examined I. ricinus individuals. Based on the nucleotide sequences of the analysed genomic fragments, most pathogens were identified as Rickettsia helvetica, while Rickettsia monacensis was revealed in one case. We have described for the first time, to our knowledge, the occurrence of this species in Poland. Both markers employed in the experiments were successful in species identification of R. helvetica. The newly described species R. monacensis may be identified by the protein-coding gene, but the ITS nucleotide sequences proved insufficient.     

Shrub clearing adversely affects the abundance of Ixodes ricinus ticks

In order to get a better understanding of the importance of vertical forest structure as a component of Ixodes ricinus tick habitat, an experiment was set up in a coniferous forest on sandy soils in northern Belgium. Ticks were sampled in six control and six treatment plots on various sampling occasions in 2008–2010. In the course of the study period, a moderate thinning was carried out in all plots and shrub clearing was performed in the treatment plots. Thinning had no effect on tick abundance, while shrub clearing had an adverse affect on the abundance of all three life stages (larva, nymph, adult) up to 2 years post-clearing. Our findings are especially relevant in the light of the ongoing efforts to improve vertical forest structure in Belgium and many other parts of Europe, which might create suitable habitats for ticks and change the epidemiology of tick-borne diseases. Also, our results indicate that shrub clearing could be applied as a tick control measure in recreational areas where there is a high degree of human-tick contact.     

Abundance of adult ticks (acari: ixodidae) in the chernobyl nuclear power plant exclusion zone

Abstract : The Chernobyl nuclear disaster resulted in contamination of vast areas in Europe. To date, there is little knowledge about the effects of radioactive contamination on tick species. We sampled ticks from vegetation and large-sized wild mammals belonging to orders Carnivora and Artiodactyla at sites with 0.76, 1.91, and 4.50?mSv/hr ionizing radiation background values in the Polesky State Radio-Ecological Reserve of the Chernobyl nuclear disaster zone in spring 2010. Altogether, 122 questing ticks were collected from vegetation. Among collected ticks, Dermacentor reticulatus (Fabricius) was, by far, the most abundant species (99.2%), followed by Ixodes ricnus (L.) (0.8%), which was collected only at the 0.76?mSv/hr site. The average sex ratio female∶male was 2.9∶1.0. In parallel with the present study, we examined 3 Sus scrofa (L.), 2 Nyctereutes procyonoides (Gray), and 1 Alces alces (L.) at the 4.50?mSv/hr site; 96 D. reticulatus ticks were found on 2 N. procyonoides specimens. The mean density and the intensity of infestation were 16 ticks per animal and 48 ticks per infested animal, respectively. Future investigations are warranted to further characterize the role of various tick vectors, vertebrate reservoirs, and diversity of tick-borne pathogens in the Chernobyl exclusion zone.     

Comparison of tick-borne microorganism communities in Ixodes spp. of the Ixodes ricinus species complex at distinct geographical regions

Characterizing the tick-borne microorganism communities of Ixodes ricinus (sheep tick) and Ixodes persulcatus (taiga tick) from the I. ricinus species complex in distinct geographical regions of Eastern Europe and European Russia, we demonstrated differences between the two ticks. Taiga ticks were more frequently mono- and co-infected than sheep ticks: 24.4 % (45/184 tested ticks) versus 17.5 % (52/297) and 4.3 % (8/184) versus 3.4 % (10/297), respectively. Ginsberg co-infection index values were significant at the various sites. Diversity of the tick-borne microorganism communities was estimated by the Shannon index, reaching values of 1.71 ± 0.46 and 1.20 ± 0.15 at the sheep-tick and the taiga-tick harbored sites, respectively. Richness of the tick-borne microorganism community in the sheep tick collection sites was about twice the value of the taiga tick collection sites. Future investigations are warranted to further characterize the peculiarities of the tick-borne microorganism communities among the ticks of the Ixodes ricinus complex.     

Tick-borne infections of animals and humans: a common ground

A wide variety of pathogens is transmitted from ticks to vertebrates including viruses, bacteria, protozoa and helminths, of which most have a life cycle that requires passage through the vertebrate host. Tick-borne infections of humans, farm and companion animals are essentially associated with wildlife animal reservoirs. While some flying insect-borne diseases of humans such as malaria, filariasis and Kala Azar caused by Leishmania donovani target people as their main host, major tick-borne infections of humans, although potentially causing disease in large numbers of individuals, are typically an infringement of a circulation between wildlife animal reservoirs and tick vectors. While new tick-borne infectious agents are frequently recognised, emerging agents of human tick-borne infections were probably circulating among wildlife animal and tick populations long before being recognised as clinical causes of human disease as has been shown for Borrelia burgdorferi sensu lato. Co-infection with more than one tick-borne infection is common and can enhance pathogenic processes and augment disease severity as found in B. burgdorferi and Anaplasma phagocytophilum co-infection. The role of wild animal reservoirs in co-infection of human hosts appears to be central, further linking human and animal tick-borne infections. Although transmission of most tick-borne infections is through the tick saliva, additional routes of transmission, shown mostly in animals, include infection by oral uptake of infected ticks, by carnivorism, animal bites and transplacentally. Additionally, artificial infection via blood transfusion is a growing threat in both human and veterinary medicine. Due to the close association between human and animal tick-borne infections, control programs for these diseases require integration of data from veterinary and human reporting systems, surveillance in wildlife and tick populations, and combined teams of experts from several scientific disciplines such as entomology, epidemiology, medicine, public health and veterinary medicine.     

Ticks (Acari: Ixodida) infesting humans in the provinces of Kelkit Valley, a Crimean-congo hemorrhagic fever endemic region in Turkey

Ticks are mandatory blood feeding ectoparasites leading transmission of various tick-borne pathogens to human and animals. Since 2002, thousands of human tick bites and numerous Crimean-Congo Hemorrhagic Fever cases have been reported in several provinces in the Kelkit Valley region in Turkey. Despite increased cases of tick bites and tick-borne diseases, no taxonomic information is available about the tick species infesting humans in the region. In the present study, a tick survey on humans was performed to determine the species composition of ticks infesting humans in several provinces of Kelkit Valley. In the survey, 1,460 ticks (721 males, 516 females and 223 nymphs) were collected from tick-infested humans. A total of 19 tick species have been found on humans in the region, including 7 Hyalomma, 2 Argas, 2 Haemaphysalis, 2 Ixodes, Dermacentor and 3 Rhipicephalus species. Infestation of Dermacentor reticulatus on humans was documented for the first time in Turkey.     

Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases?

The impact of climate change on vector-borne infectious diseases is currently controversial. In Europe the primary arthropod vectors of zoonotic diseases are ticks, which transmit Borrelia burgdorferi sensu lato (the agent of Lyme disease), tick-borne encephalitis virus and louping ill virus between humans, livestock and wildlife. Ixodes ricinus ticks and reported tick-borne disease cases are currently increasing in the UK. Theories for this include climate change and increasing host abundance. This study aimed to test how I. ricinus tick abundance might be influenced by climate change in Scotland by using altitudinal gradients as a proxy, while also taking into account the effects of hosts, vegetation and weather effects. It was predicted that tick abundance would be higher at lower altitudes (i.e. warmer climates) and increase with host abundance. Surveys were conducted on nine hills in Scotland, all of open moorland habitat. Tick abundance was positively associated with deer abundance, but even after taking this into account, there was a strong negative association of ticks with altitude. This was probably a real climate effect, with temperature (and humidity, i.e. saturation deficit) most likely playing an important role. It could be inferred that ticks may become more abundant at higher altitudes in response to climate warming. This has potential implications for pathogen prevalence such as louping ill virus if tick numbers increase at elevations where competent transmission hosts (red grouse Lagopus lagopus scoticus and mountain hares Lepus timidus) occur in higher numbers.     

Blood-sucking ticks (Acarina,Ixodoidea) as an essential component of the urban environment

The problem of urban ticks has arisen from the increased rate of urbanization since WWII. Expansion of municipal boundaries encompasses adjacent territories, so that large areas of wilderness together with all their inhabitants get incorporated into city limits. Current strategies of biodiversity conservation include the creation of green corridors and other forms of connectivity between wilderness and urban areas as well as between green patches within cities. All this allows various mammals and birds to migrate from their native habitats into and between various parts of the cities and to establish permanent urban populations. Medium-sized and larger animals provide adult ticks with blood meal, thus creating suitable conditions for the establishment and persistence of tick populations. Independent tick populations can exist in urban forests, parks, private properties, old cemeteries, etc. Over the last decades, the tick populations that originated from those in natural habitats around the cities have become a permanent component of urban fauna. Among such ticks, the castor bean tick Ixodes ricinus is the most important species for European cities, while the deer tick I. scapularis is of great significance for the East Coast of the United States. The taiga tick I. persulcatus is the most important species for the Russian cities and towns within its range. All these and some other ticks aggressively attack humans and their pets inside cities. The tick species especially well adapted to urban life are those which can live and reproduce in buildings. The brown dog tick Rhipicephalus sanguineus (family Ixodidae), the pigeon ticks from the reflexus group of the genus Argas, and Ornithodoros ticks (family Argasidae), which form urban and semi-urban populations, are the main urban tick pests and vectors. House infestation by ticks can lead to human infection with tick-borne pathogens or severe allergic reactions. Some tick hosts, mammals as well as birds, maintain tick-transmitted pathogens and serve as competent reservoir hosts. Urban populations of these animals can participate in the circulation of some pathogens within cities. Thus, the enlargement of urban green areas followed by their population by wild mammals and birds create good opportunities for the establishment of urban populations of tick vectors with the resulting threat to the health of urban dwellers and their pets. At the same time, our understanding of the real scope and complexity of the problem of urban ticks is far from being sufficient. Finding the ways of protecting the environment without increasing the risk to human health in modern cities is a pressing and challenging problem of our time.     

Emerging rickettsioses

Ticks are known to carry and transmit a number of microbial agents that cause diseases in humans and animals. Among these are members of the order Rickettsiales (alpha-proteobacteria), which include the genera Rickettsia and Ehrlichia. The most common and well-known Rickettsial human disease in Europe is Mediterranean Spotted Fever (MSF), caused by Rickettsia conorii. In recent years, a number of new Rickettsia species have been discovered in Europe, some of which have been shown to be pathogenic to humans. These discoveries have been facilitated by use of sequence-based molecular identification techniques. In Italy, it is generally believed that R. conorii is the only Rickettsia species present, and clinical tests for MSF rely on antigens raised against this bacterium. We are currently undertaking a molecular screening study of Rickettsiales-bacteria in ticks from various regions of Italy, to check for the potential presence of species from this order recently discovered in other parts of Europe. So far, we have identified a number of additional species in ticks collected from northern, central and southern regions. These include the known pathogens R. helvetica and R. slovaca as well as two species which may or may not be of medical relevance: R. monacensis and R. sp. IRS4. As a part of this survey, we have identified a novel alphaproteobacterium from the medically important tick Ixodes ricinus. This bacterium, tentatively named IricES1, has the unusual property of existing within the mitochondria, as well as the cytoplasm, of ovarian cells. To our knowledge, this is the only known example of a bacterium that is able to enter the mitochondria of animals. Our recently published electron microscopic data indicates that the bacterium enters mitochondria between the inner and outer membranes, and then proceeds to consume the inner mitochondrial matrix. We will present further data on this bacterium, including: 1) its phylogenetic position based on various molecular sequences, 2) its localization within the tick based on in situ hybridization; 3) its distribution among tick populations in Europe; 4) preliminary data on attempts at culturing this bacterium in a variety of cell types. Possible interactions between the bacterium and its host will be discussed. Ticks are known to carry and transmit a number of microbial agents that cause diseases in humans and animals. Among these are members of the order Rickettsiales (alpha-proteobacteria), which include the genera Rickettsia and Ehrlichia. The most common and well-known Rickettsial human disease in Europe is Mediterranean Spotted Fever (MSF), caused by Rickettsia conorii. In recent years, a number of new Rickettsia species have been discovered in Europe, some of which have been shown to be pathogenic to humans. These discoveries have been facilitated by use of sequence-based molecular identification techniques. In Italy, it is generally believed that R. conorii is the only Rickettsia species present, and clinical tests for MSF rely on antigens raised against this bacterium. We are currently undertaking a molecular screening study of Rickettsiales-bacteria in ticks from various regions of Italy, to check for the potential presence of species from this order recently discovered in other parts of Europe. So far, we have identified a number of additional species in ticks collected from northern, central and southern regions. These include the known pathogens R. helvetica and R. slovaca as well as two species which may or may not be of medical relevance: R. monacensis and R. sp. IRS4. As a part of this survey, we have identified a novel alphaproteobacterium from the medically important tick Ixodes ricinus. This bacterium, tentatively named IricES1, has the unusual property of existing within the mitochondria, as well as the cytoplasm, of ovarian cells. To our knowledge, this is the only known example of a bacterium that is able to enter the mitochondria of animals. Our recently published electron microscopic data indicates that the bacterium enters mitochondria between the inner and outer membranes, and then proceeds to consume the inner mitochondrial matrix. We will present further data on this bacterium, including: 1) its phylogenetic position based on various molecular sequences, 2) its localization within the tick based on in situ hybridization; 3) its distribution among tick populations in Europe; 4) preliminary data on attempts at culturing this bacterium in a variety of cell types. Possible interactions between the bacterium and its host will be discussed.