The role of blood-sucking ticks and insects in natural foci of infections

During 60 years passed after the creation of the conception on natural focus of human infections by the academician E. N. Pavlovski? our knowledge on a role of blood-sucking insects and ticks in this phenomenon have been significantly enlarged. It has been recovered, that these arthropods serve not only as vectors of infection agents, but also as natural reservoirs and amplificators of these agents. In the process of the infection agent circulation in the natural focus there are several additional pathways of circulations without a participation of vertebrates. These pathways are as follows: the dispersion of infection agent in cases of simultaneous feeding of infected and "clean" ticks, and also the sexual, transovarial and transphase transmissions of pathogens. These mechanism of circulation are most often occur in the ixodid ticks, which can play the main role in supporting the infection agent in the focus.     

Significance of ixodid tick (Parasitiformes,Ixodidae) population structure for maintenance of natural foci of infection

Basic postulates of the theory of natural focality of infections are considered in terms of modern ecological parasitology using the example of Ixodes ricinus and I. persulcatus ticks, the main vectors of tickborne encephalitis and borrelioses in Eurasia. Consideration is given to data on the population structure of ticks, their distribution in ecosystems, abundance, mortality at different stages of the life cycle, seasonal dynamics of activity, occurrence on different vertebrate species, relationships with potential hosts, and connections agents of infections. Due to long individual life span and development of one generation over 3–6 years, tick vector provide not only for transmission of pathogens, but also for their long-term storage and amplification. Several alternative routes of tick infection of ticks provide for pathogen exchange between individuals at different phases of development within one generation and between feeding ticks of different generations.     

The possibility of the detection of one more tick-borne infection--babesiosis--on the territory of Russia

A total of 739 taiga ticks of ixodes persulcatus species, obtained in the recreational zone of St. Petersburg, were studied for the presence of Babesia sp. with polymerase chain reaction. All these ticks underwent the preliminary examination for the presence of Borrelia (3 species), Ehrlichia (2 species) and tick-borne encephalitis (TBE) virus. In 7 cases Babesia were detected among 413 ticks containing other pathogens. Among 326 ticks no Babesia were detected, as well as no other pathogens. All ticks having Babesia were also found to contain Borrelia species: B. afzelii, B. garinii, or both (1 case). In one female tick, in addition to Babesia, also B. garinii and TBE virus were determined. The data thus obtained should draw special attention not only of parasitologists, epidemiologists and microbiologists studying ticks obtained from natural sources, but also of clinicists who should consider the possibility of mixed infection, when one infection may mask the presence of some other infection, in particular babesiosis. Due to rare occurrence of Babesia in ticks and the presence of mixed infection difficulties may arise in the detection of Babesia.     

Associations Between Coinfection Prevalence of <Emphasis Type="Italic">Borrelia lusitaniae</Emphasis>, <Emphasis Type="Italic">Anaplasma</Emphasis> sp., and <Emphasis Type="Italic">Rickettsia</Emphasis> sp. in Hard Ticks Feeding on Reptile Hosts

An increasing number of studies reveal that ticks and their hosts are infected with multiple pathogens, suggesting that coinfection might be frequent for both vectors and wild reservoir hosts. Whereas the examination of associations between coinfecting pathogen agents in natural host–vector–pathogen systems is a prerequisite for a better understanding of disease maintenance and transmission, the associations between pathogens within vectors or hosts are seldom explicitly examined. We examined the prevalence of pathogen agents and the patterns of associations between them under natural conditions, using a previously unexamined host–vector–pathogen system—green lizards Lacerta viridis, hard ticks Ixodes ricinus, and Borrelia, Anaplasma, and Rickettsia pathogens. We found that immature ticks infesting a temperate lizard species in Central Europe were infected with multiple pathogens. Considering I. ricinus nymphs and larvae, the prevalence of Anaplasma, Borrelia, and Rickettsia was 13.1% and 8.7%, 12.8% and 1.3%, and 4.5% and 2.7%, respectively. The patterns of pathogen prevalence and observed coinfection rates suggest that the risk of tick infection with one pathogen is not independent of other pathogens. Our results indicate that Anaplasma can play a role in suppressing the transmission of Borrelia to tick vectors. Overall, however, positive effects of Borrelia on Anaplasma seem to prevail as judged by higher-than-expected Borrelia–Anaplasma coinfection rates.     

Use of partially engorged female ticks as laboratory animals in microbiological research

Abstract. Partially engorged female ticks were used as laboratory animals in microbiological research. The ticks, which were inoculated intracoelomally, became a convenient substrate for the detection of viruses, rickettsiae and protozoal parasites. This research concerned the isolation of newly recovered micro-organisms, the study of development, structure and distribution of microbial agents in ticks, and the study of their interaction with other pathogens or symbionts during mixed infection in a tick body. The isolation and maintenance of Rickettsiella phytoseiuli , the organism not of tick-borne origin, was achieved. For use in Central Europe the tick Dermacentor reticulatus is recommended for the above investigations.     

Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records

Ticks are often infected with more than one pathogen, and several field surveys have documented nonrandom levels of coinfection. Levels of coinfection by pathogens in four tick species were analyzed using published infection data. Coinfection patterns of pathogens in field-collected ticks include numerous cases of higher or lower levels of coinfection than would be expected due to chance alone, but the vast majority of these cases can be explained on the basis of vertebrate host associations of the pathogens, without invoking interactions between pathogens within ticks. Nevertheless, some studies have demonstrated antagonistic interactions, and some have suggested potential mutualisms, between pathogens in ticks. Negative or positive interactions between pathogens within ticks can affect pathogen prevalence, and thus transmission patterns. Probabilistic projections suggest that the effect on transmission depends on initial conditions. When the number of tick bites is relatively low (e.g., for ticks biting humans) changes in prevalence in ticks are predicted to have a commensurate effects on pathogen transmission. In contrast, when the number of tick bites is high (e.g., for wild animal hosts) changes in pathogen prevalence in ticks have relatively little effect on levels of transmission to reservoir hosts, and thus on natural transmission cycles.     

Mixed infection by tick-borne encephalitis virus and Borrelia in ticks

To investigate the relationships between tick-borne encephalitis (TBE) virus and the bacterial spirochaete Borrelia burgdorferi sensu lato in vectors with mixed infections, unfed adult Ixodes persulcatus ticks were collected by flagging from vegetation in southern-taiga forests of the Pre-Urals region of Russia where both infections circulate sympatrically. Prevalences of TBE and Borrelia infections in a total of 4234 ticks were compared over 5 years. No significant differences were revealed between the prevalence of Borrelia infection in ticks with and without TBE virus (29.4+/-7.8% vs 23+/-3.6%), or between the prevalence of TBE virus infection in ticks with and without Borrelia (24.0+/-6.6% vs 18.4+/-3.4%). In ticks with mixed infection (40/689 = 5.8%), concentrations of TBE virus and Borrelia were not significantly correlated with one another. Field observations showed parallel trends in the prevalence of these pathogens in tick populations from year to year (1993-1997) indicating that, in I. persulcatus with mixed infection, Borrelia and TBE virus do not seem to interfere with each other and are apparently not involved in any antagonistic relationships.     

Experimental and Natural Infections of Goats with Severe Fever with Thrombocytopenia Syndrome Virus: Evidence for Ticks as Viral Vector

Background

Severe fever with thrombocytopenia syndrome virus (SFTSV), the causative agent for the fatal life-threatening infectious disease, severe fever with thrombocytopenia syndrome (SFTS), was first identified in the central and eastern regions of China. Although the viral RNA was detected in free-living and parasitic ticks, the vector for SFTSV remains unsettled.

Methodology/Principal Findings

Firstly, an experimental infection study in goats was conducted in a bio-safety level-2 (BSL-2) facility to investigate virus transmission between animals. The results showed that infected animals did not shed virus to the outside through respiratory or digestive tract route, and the control animals did not get infected. Then, a natural infection study was carried out in the SFTSV endemic region. A cohort of naïve goats was used as sentinel animals in the study site. A variety of daily samples including goat sera, ticks and mosquitoes were collected for viral RNA and antibody (from serum only) detection, and virus isolation. We detected viral RNA from free-living and parasitic ticks rather than mosquitoes, and from goats after ticks’ infestation. We also observed sero-conversion in all members of the animal cohort subsequently. The S segment sequences of the two recovered viral isolates from one infected goat and its parasitic ticks showed a 100% homology at the nucleic acid level.

Conclusions/Significance

In our natural infection study, close contact between goats does not appear to transmit SFTSV, however, the naïve animals were infected after ticks’ infestation and two viral isolates derived from an infected goat and its parasitic ticks shared 100% of sequence identity. These data demonstrate that the etiologic agent for goat cohort’s natural infection comes from environmental factors. Of these, ticks, especially the predominant species Haemaphysalis longicornis, probably act as vector for this pathogen. The findings in this study may help local health authorities formulate and focus preventive measures to contain this infection.     

Ticks (Acari: Ixodoidea) in China: Geographical distribution,host diversity,and specificity

Ticks are obligate blood‐sucking ectoparasites, which not only directly damage through bites but also transmit many pathogens. China has a high diversity of tick species, 125 species have been reported, including 111 hard tick and 14 soft tick species. Many of the ticks are important vectors of pathogens, resulting in zoonoses. The dynamics of ticks are affected by both the host and habitat environment. However, systematic studies on the geographical distribution, host diversity, and specificity of ticks are limited in China. To achieve this goal, the relevant available data were summarized and analyzed in this study. Ticks are distributed in all parts of China and Xinjiang has the most records of ticks. The distribution of ticks in adjacent areas is similar, indicating that the habitat environment affects their distribution. Most ticks are widely distributed, whereas some species are endemic to their distributed regions. Ticks are parasitic on mammals, birds, and reptiles, of which mammals are the main host species. Overall, most ticks parasitize different hosts, only a few ticks have strict host specificity, such as ticks that are specifically parasitic on reptiles and bats. In addition, environmental changes and control efforts also influence the dynamics of ticks. These results can better reveal tick biological traits and are valuable for tick control.     

Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia

The list of tick-borne pathogens is long, varied and includes viruses, bacteria, protozoa and nematodes. As all of these agents can exist in ticks, their co-infections have been previously reported. We studied co-infections of emerging bacterial pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Francisella tularensis) in Ixodes ricinus ticks in Serbia. Using PCR technique, we detected species-specific sequences, rrf-rrl rDNA intergenic spacer for B. burgdorferi s.l., p44/msp2 paralogs for A. phagocytophilum, and the 17 kDa lipoprotein gene, TUL4, for F. tularensis, respectively, in total DNA extracted from the ticks. Common infections with more than one pathogen were detected in 42 (28.8%) of 146 infected I. ricinus ticks. Co-infections with two pathogens were present in 39 (26.7%) of infected ticks. Simultaneous presence of A. phagocytophilum and different genospecies of B. burgdorferi s.l. complex was recorded in 16 ticks, co-infection with different B. burgdorferi s. l. genospecies was found in 15 ticks and eight ticks harbored mixed infections with F. tularensis and B. burgdorferi s.l. genospecies. Less common were triple pathogen species infections, detected in three ticks, one infected with A. phagocytophilum / B. burgdorferi s.s. / B. lusitaniae and two infected with F. tularensis / B. burgdorferi s.s. / B. lusitaniae. No mixed infections of A. phagocytophilum and F. tularensis were detected.     

The characteristics of the ixodid tick-vertebrate animal parasitic system]

The parasitic system ixodid tick (parasite)--vertebrate animal (host) is relatively stable in space and time. Equilibrium state in the system is maintained at the low levels of the hosts' infection and moderate intensity of their immunity. Parasite sensitizes the host's organism at the stage of feeding on antigens of its saliva and the host develops different degrees of resistance preventing the subsequent individuals of ticks from normal feeding. Antitick immunity is species specific. Its intensity is defined by the species belonging of the parasite and host, intensity and intervals between infections, availability of "anti-immune mechanisms" in tick and by many other factors, which are realized at the feeding stage. Regulation of the number of ticks, depending on their abundance in the host's population, is attained due to the oversparse, close to negative binomial distribution on hosts. This mechanism functions on the principle of feedback, so that at the excessive number of the parasite some individuals in the host's population, which are especially subjected to infection, do not cope with parasitic burden and die. However, ticks, which failed to finish their feeding and represent a disproportionately great part of the whole parasite's population, die together with them and the parasitic system quickly restores its stability. In anthropocoenoses and ecosystems at different stages of anthropogenic transformation mutual regulation mechanisms of the parasite and host number break down. As a consequence, extremely high rises in the number of ticks and epizootics of agricultural animals associated with them can occur.     

Fungal Biocontrol of Acari

Mites and ticks are susceptible to pathogenic fungi, and there are opportunities to exploit these micro-organisms for biological control. We have collated records of 58 species of fungi infecting at least 73 species of Acari, either naturally or in experiments. Fungal pathogens have been reported to kill representatives of all three orders of the Actinotrichida (the Astigmata, Oribatida and Prostigmata) and the Ixodida and Mesostigmata in the Anactinotrichida. Most reports concern infections in the Prostigmata, particularly in the families Tetranychidae and Eriophyidae. Two species of Acari-specific pathogens - Hirsutella thompsonii and Neozygites floridana - are important natural regulators of pestiferous eriophyoid and tetranychid mites respectively. Research has been done to understand the factors leading to epizootics of these fungi and to conserve and enhance natural pest control. Hirsutella thompsonii was also developed as the commercial product Mycar for the control of eriophyoid mites on citrus, but was withdrawn from sale in the 1980s, despite some promising effects in the field. Beauveria bassiana , Metarhizium anisopliae, Paecilomyces farinosus, Paecilomyces fumosoroseus and Verticillium lecanii infect ixodid ticks in nature, and B. bassiana and M. anisopliae are being studied as biological control agents of cattle ticks in Africa and South America. Beauveria bassiana also has potential as a mycopesticide of the two-spotted spider mite, Tetranychus urticae . There is scope to develop fungal biocontrol agents against a range of acarine pests, both as stand-alone treatments and for use in integrated pest management. Further research is required to clarify the taxonomic status of fungal pathogens of Acari, to study their ecosystem function, and to develop efficient mass production systems for species of Hirsutella and Neozygites .     

Predators,parasitoids and pathogens of ticks: A review

Research conducted on natural enemies of ticks, namely predators, parasitoids and pathogens, is reviewed. Predators include ants, birds, rodents, lizards, shrews, spiders and domestic chickens. All the known parasitoids are hymenopteran wasps belonging to the genera Ixodiphagus and Hunterellus. The work so far done on bacteria, fungi, viruses and rickettsiae which are pathogenic to ticks is reviewed, both with regard to experimental infections and natural infections. The possibilities of using natural enemies as biological control agents of ticks are discussed.     

Elasticity analysis in epidemiology: an application to tick-borne infections

The application of projection matrices in population biology to plant and animal populations has a parallel in infectious disease ecology when next-generation matrices (NGMs) are used to characterize growth in numbers of infected hosts ( R ₀). The NGM is appropriate for multi-host pathogens, where each matrix element represents the number of cases of one type of host arising from a single infected individual of another type. For projection matrices, calculations of the sensitivity and elasticity of the population growth rate to changes in the matrix elements has generated insight into plant and animal populations. These same perturbation analyses can be used for infectious disease systems. To illustrate this in detail we parameterized an NGM for seven tick-borne zoonoses and compared them in terms of the contributions to R ₀ from three different routes of transmission between ticks, and between ticks and vertebrate hosts. The definition of host type may be the species of the host or the route of infection, or, as was the case for the set of tick-borne pathogens, a combination of species and the life stage at infection. This freedom means that there is a broad range of disease systems and questions for which the methodology is appropriate.     

Restriction of Francisella novicida Genetic Diversity during Infection of the Vector Midgut

The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as “ecological filters” for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.     

Vector-host interactions in disease transmission

Tick-borne spirochetes include borreliae that cause Lyme disease and relapsing fever in humans. They survive in a triangle of parasitic interactions between the spirochete and its vertebrate host, the spirochete and its tick vector, and the host and the tick. Until recently, the significance of vector-host interactions in the transmission of arthropod-borne disease agents has been overlooked. However, there is now compelling evidence that the pharmacological activity of tick saliva can have a profound effect on pathogen transmission both from infected tick to uninfected host, and from infected host to uninfected tick. The salivary glands of ticks provide a pharmacopoeia of anti-inflammatory, anti-haemostatic and anti-immune molecules. These include bioactive proteins that control histamine, bind immunoglobulins, and inhibit the alternative complement cascade. The effect of these molecules is to provide a privileged site at the tick-host interface in which borreliae and other tick-borne pathogens are sheltered from the normal innate and acquired host immune mechanisms that combat infections. Understanding the key events at the tick vector-host interface, that promote spirochete infection and transmission, will provide a better understanding of the epidemiology and ecology of these important human pathogens.     

Detection of DNA erlichia and anaplasma in ticks Ixodes trianguliceps in Tyumen Province

The data on the study of Ixodes trianguliceps Bir. collected from small mammals in the southern taiga forests of Tyumen Province with the PCR-hybridization with fluorescent detection method are given. DNA of Erlichua and Anaplasma was revealed in ticks of this species for the first time; mixed infection with both these pathogens was also demonstrated.     

Mixed infections, cryptic diversity, and vector-borne pathogens: evidence from Polygenis fleas and Bartonella species

Coinfections within hosts present opportunities for horizontal gene transfer between strains and competitive interactions between genotypes and thus can be a critical element of the lifestyles of pathogens. Bartonella spp. are Alphaproteobacteria that parasitize mammalian erythrocytes and endothelial cells. Their vectors are thought to be various biting arthropods, such as fleas, ticks, mites, and lice, and they are commonly cited as agents of various emerging diseases. Coinfections by different Bartonella strains and species can be common in mammals, but little is known about specificity and coinfections in arthropod vectors. We surveyed the rate of mixed infections of Bartonella in flea vectors (Polygenis gwyni) parasitizing cotton rats (Sigmodon hispidus) in which previous surveys indicated high rates of infection. We found that nearly all fleas (20 of 21) harbored one or more strains of Bartonella, with rates of coinfection approaching 90%. A strain previously identified as common in cotton rats was also common in their fleas. However, another common strain in cotton rats was absent from P. gwyni, while a rare cotton rat strain was quite common in P. gwyni. Surprisingly, some samples were also coinfected with a strain phylogenetically related to Bartonella clarridgeiae, which is typically associated with felids and ruminants. Finally, a locus (pap31) that is characteristically borne on phage in Bartonella was successfully sequenced from most samples. However, sequence diversity in pap31 was novel in the P. gwyni samples, relative to other Bartonella previously typed with pap31, emphasizing the likelihood of large reservoirs of cryptic diversity in natural populations of the pathogen.     

Tissue Distribution of the Ehrlichia muris-Like Agent in a Tick Vector

Human pathogens transmitted by ticks undergo complex life cycles alternating between the arthropod vector and a mammalian host. While the latter has been investigated to a greater extent, examination of the biological interactions between microbes and the ticks that carry them presents an equally important opportunity for disruption of the disease cycle. In this study, we used in situ hybridization to demonstrate infection by the Ehrlichia muris-like organism, a newly recognized human pathogen, of Ixodes scapularis ticks, a primary vector for several important human disease agents. This allowed us to assess whole sectioned ticks for the patterns of tissue invasion, and demonstrate generalized dissemination of ehrlichiae in a variety of cell types and organs within ticks infected naturally via blood feeding. Electron microscopy was used to confirm these results. Here we describe a strong ehrlichial affinity for epithelial cells, neuronal cells of the synganglion, salivary glands, and male accessory glands.     

Pathogen prevalence in ticks collected from the vegetation and livestock in Nigeria

Ticks are important disease vectors that can cause considerable economic losses by affecting animal health and productivity, especially in tropical and subtropical regions. In this study, we investigated the prevalence and diversity of bacterial and protozoan tick-borne pathogens in ticks collected from the vegetation and cattle in Nigeria by PCR. The infection rates of questing ticks were 3.1% for Rickettsia species, 0.1% for Coxiella burnetii and 0.4% for Borrelia species. Other pathogens, such as Babesia, Theileria, Anaplasma, and Ehrlichia species, were not detected in ticks from the vegetation. Feeding ticks collected from cattle displayed infection rates of 12.5% for Rickettsia species, 14% for Coxiella burnetii, 5.9% for Anaplasma species, 5.1% for Ehrlichia species, and 2.9% for Theileria mutans. Babesia and Borrelia species were not detected in ticks collected from cattle. Mixed infections were found only in feeding ticks and mainly Rickettsia species and Coxiella burnetii were involved. The diversity of tick-borne pathogens in Nigeria was higher in feeding than in questing ticks, suggesting that cattle serve as reservoirs for at least some of the pathogens studied, in particular C. burnetii. The total estimated herd infection rates of 20.6% for a Rickettsia africae-like species, 27% for Coxiella burnetii, and 8.5% for Anaplasma marginale/centrale suggest that these pathogens may have considerable implications for human and animal health.