Agustín Estrada-Peña

Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe

Many factors are involved in determining the latitudinal and altitudinal spread of the important tick vector Ixodes ricinus (Acari: Ixodidae) in Europe, as well as in changes in the distribution within its prior endemic zones. This paper builds on published literature and unpublished expert opinion from the VBORNET network with the aim of reviewing the evidence for these changes in Europe and discusses the many climatic, ecological, landscape and anthropogenic drivers. These can be divided into those directly related to climatic change, contributing to an expansion in the tick’s geographic range at extremes of altitude in central Europe, and at extremes of latitude in Scandinavia; those related to changes in the distribution of tick hosts, particularly roe deer and other cervids; other ecological changes such as habitat connectivity and changes in land management; and finally, anthropogenically induced changes. These factors are strongly interlinked and often not well quantified. Although a change in climate plays an important role in certain geographic regions, for much of Europe it is non-climatic factors that are becoming increasingly important. How we manage habitats on a landscape scale, and the changes in the distribution and abundance of tick hosts are important considerations during our assessment and management of the public health risks associated with ticks and tick-borne disease issues in 21st century Europe. Better understanding and mapping of the spread of I. ricinus (and changes in its abundance) is, however, essential to assess the risk of the spread of infections transmitted by this vector species. Enhanced tick surveillance with harmonized approaches for comparison of data enabling the follow-up of trends at EU level will improve the messages on risk related to tick-borne diseases to policy makers, other stake holders and to the general public.

Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission.

In this article, literature records of argasid and ixodid ticks feeding on humans worldwide are provided in view of increased awareness of risks associated with tick bites. Ticks can cause paralyses, toxicoses, allergic reactions and are vectors of a broad range of viral, rickettsial, bacterial and protozoan pathogens. Approximately 12 argasid species (Argas and Ornithodos) are frequently found attached to humans who intrude into tick-infested caves and burrows. Over 20 ixodid tick species are often found on humans exposed to infested vegetation: four of these are Amblyomma species, 7 Dermacentor spp., 3 Haemaphysalis spp., 2 Hyalomma spp. and 6 Ixodes species. Personal protection methods, such as repellents and acaricide-impregnated clothing are advised to minimize contact with infected ticks. Acaricidal control of ixodid ticks is impractical because of their wide distribution in forested areas, but houses infested with soft ticks can be sprayed with acaricidal formulations. Attached ticks should be removed without delay. The best way is to grasp the tick as close to the skin as possible with fine tweezers and pull firmly and steadily without twisting. Finally, despite the fact that most people who are bitten destroy the offending tick in disgust, it is recommended that they preserve specimens in ethanol for taxonomic identification and detection of pathogens by molecular methods.

Ticks (Ixodidae) on humans in South America

Twenty eight species of Ixodidae have been found on man in South America (21 Amblyomma, 1 Boophilus, 2 Dermacentor, 2 Haemaphysalis, 1 Ixodes and 1 Rhipicephalus species). Most of them are rarely found on man. However, three species frequently parasitize humans in restricted areas of Argentina (A. neumanni reported from 46 localities), Uruguay (A. triste from 21 sites) and Argentina–Brazil (A. parvum from 27 localities). The most widespread ticks are A. cajennense (134 localities in Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Suriname and Venezuela), A. ovale (37 localities in Argentina, Brazil, Ecuador, French Guiana, Guyana, Paraguay, Suriname and Venezuela) and A. oblongoguttatum (28 sites in Brazil, Colombia, French Guiana, Guyana, Suriname and Venezuela). Amblyomma aureolatum (18 localities in Argentina, Brazil, French Guiana and Paraguay), A. cajennense, and A. triste are vectors of rickettsioses to man in South America. A better understanding of the respective roles of these and other tick species in transmitting pathogens to humans will require further local investigations. Amblyomma ticks should be the main subjects of these studies followed by species of Boophilus, Dermacentor, Haemaphysalis and Rhipicephalus species. In contrast with North America, Europe and Asia, ticks of the genus Ixodes do not appear to be major players in transmitting diseases to human. Indeed, there is only one record of an Ixodes collected while feeding on man for all South America.

Bovine piroplasms in Minorca (Balearic Islands, Spain): a comparison of PCR-based and light microscopy detection.

The present study provides the first epidemiological data regarding infection by Theileria and Babesia piroplasms in cattle in Minorca. More than 94% of the studied animals were positive for the presence of Theileria sp., and of those, 41.3% were positive for the presence of Theileria annulata. These results indicate that the prevalence of Mediterranean theileriosis caused by T. annulata is very high in Minorcan dairy farms and that other Theileria sp. are also present in the area. The prevalence of infection was similar throughout the study indicating an endemic situation in this island. The use of PCR resulted in significantly higher efficacy of detection of Theileria sp. compared to microscopical observation (MO) of blood smears and allowed the specific discrimination between pathogenic and non-pathogenic theilerias which cannot be accomplished by traditional diagnosis by MO. Babesia infection in the area was mainly due to Babesia bigemina (6.0% of the studied animals were infected), while one animal (0.75%) was found to be infected by Babesia bovis. It was observed that 31% of animals infected with B. bigemina had a concurrent infection of T. annulata. PCR also resulted in a significantly higher efficacy of detection of Babesia sp. compared to MO when infection levels were higher, towards the end of the study period. The results clearly demonstrate that parasitic infection by piroplasms, especially Theileria sp. is common and endemic in the island of Minorca and that PCR is the optimal approach for the detection and discrimination of these important parasites.

The Amblyomma maculatum Koch, 1844 (Acari: Ixodidae: Amblyomminae) tick group: diagnostic characters, description of the larva of A. parvitarsum Neumann, 1901, 16S rDNA sequences, distribution and hosts.

A review of the largely confused Amblyomma maculatum Koch, 1844 tick group of the subgenus Anastosiella Santos Dias, 1963 (A. neumanni Ribaga, 1902, A. maculatum, A. parvitarsum Neumann, 1901, A. tigrinum Koch, 1844 and A. tristeKoch, 1844) is presented together with a discussion of the diagnostic characters used for the determination of adults, nymphs and, to a lesser extent, larvae. A key for this tick group is produced, including the description of the larva of A. parvitarsum, 1901. Sequences of 16S rDNA are obtained and compared with other Amblyomma spp., including two other species currently in Anastosiella but in the ovaletick group, A. ovale Koch, 1844 and A. aureolatum(Pallas, 1772). According to the morphology and the rDNA sequences, the maculatum group is reduced to A. maculatum (Neotropical-Nearctic), A. tigrinum (Neotropical) and A. triste (Neotropical) A. neumanni and A. parvitarsum are excluded from the subgenus. The distribution is sympatric in northern South America from where A. maculatumreaches the southern Nearctic and the range of A. tigrinum extends to the southern Neotropics. These species have been found on several domestic and wild vertebrates. A. triste and A. tigrinum have been also found on man. Their role as vectors of pathogens deserves further investigation.

Lyme borreliosis habitat assessment

Tick ecologists throughout Europe provided descriptions of Lyme borreliosis habitats according to a standardised format and data for 105 habitats in 16 countries were received. The data showed that high risk situations, as defined by the presence of large numbers of B. burgdorferi sensu lato-infected nymphal I. ricinus, occur in heterogeneous deciduous woodland, usually with a recreational function and with a diverse fauna, usually including deer. Large numbers of ticks occurred in some other habitats, but infection prevalence was usually low. The situation for adult I. ricinus was similar but less clearly defined. Tick infection rates were found to be lower in western Europe than in the east, and the infection rate in I. persulcatus, the most easterly vector species, was markedly higher than in I. ricinus. In the vast majority of habitats the infection rate in adult I. ricinus was greater than in nymphs. Larvae were rarely found to be infected.

Impact of climate trends on tick-borne pathogen transmission.

Recent advances in climate research together with a better understanding of tick–pathogen interactions, the distribution of ticks and the diagnosis of tick-borne pathogens raise questions about the impact of environmental factors on tick abundance and spread and the prevalence and transmission of tick-borne pathogens. While undoubtedly climate plays a role in the changes in distribution and seasonal abundance of ticks, it is always difficult to disentangle factors impacting on the abundance of tick hosts from those exerted by human habits. All together, climate, host abundance, and social factors may explain the upsurge of epidemics transmitted by ticks to humans. Herein we focused on tick-borne pathogens that affect humans with epidemic potential. Borrelia burgdorferi s.l. (Lyme disease), Anaplasma phagocytophilum (human granulocytic anaplasmosis), and tick-borne encephalitis virus (tick-borne encephalitis) are transmitted by Ixodes spp. Crimean–Congo hemorrhagic fever virus (Crimean–Congo hemorrhagic fever) is transmitted by Hyalomma spp. In this review, we discussed how vector tick species occupy the habitat as a function of different climatic factors, and how these factors impact on tick survival and seasonality. How molecular events at the tick–pathogen interface impact on pathogen transmission is also discussed. Results from statistically and biologically derived models are compared to show that while statistical models are able to outline basic information about tick distributions, biologically derived models are necessary to evaluate pathogen transmission rates and understand the effect of climatic variables and host abundance patterns on pathogen transmission. The results of these studies could be used to build early alert systems able to identify the main factors driving the subtle changes in tick distribution and seasonality and the prevalence of tick-borne pathogens.

Effects of environmental change on zoonotic disease risk: an ecological primer

Impacts of environmental changes on zoonotic disease risk are the subject of speculation, but lack a coherent framework for understanding environmental drivers of pathogen transmission from animal hosts to humans. We review how environmental factors affect the distributions of zoonotic agents and their transmission to humans, exploring the roles they play in zoonotic systems. We demonstrate the importance of capturing the distributional ecology of any species involved in pathogen transmission, defining the environmental conditions required, and the projection of that niche onto geography. We further review how environmental changes may alter the dispersal behaviour of populations of any component of zoonotic disease systems. Such changes can modify relative importance of different host species for pathogens, modifying contact rates with humans.

Crimean-Congo Hemorrhagic Fever Virus in Ticks, Southwestern Europe, 2010

To the Editor: Crimean-Congo hemorrhagic fever virus (CCHFV; family Bunyaviridae, genus Nairovirus) causes outbreaks of severe hemorrhagic fever in humans, with case-fatality rates <30% (1,2). The disease was initially recognized by Russian scientists in the 1940s (3), and the virus was first isolated in the Democratic Republic of Congo some years later (4). CCHFV is reported throughout broad regions of Africa, Europe, the Middle East, and Asia. Reports linking transmission of the virus with an infected vector have involved ticks of the genus Hyalomma (5). It appears that maintenance of active foci of CCHFV in the field is dependent on Hyalomma spp., even within periods of silent activity. Several vertebrates are involved in the natural transmission cycle (6). Transmission of CCHFV to humans occurs through tick bites, direct contact with blood or tissues of infected animals, person-to-person spread, or by nosocomial infection (1). In southeastern Europe, the Balkans are the known western limit for CCHFV (7). This finding is of special interest because Hyalomma marginatum, the main tick vector in the western Paleartic (an ecozone that includes temperate and cold areas of Eurasia and North Africa and several archipelagos and islands in the Atlantic and Pacific Oceans), is common throughout the Mediterranean Basin (7), where clinical cases of the disease or the virus have not been reported. Unsupported claims of the effects of climate on virus distribution have been reported but never empirically demonstrated (8). We report the detection of CCHFV in ticks collected in southwestern Europe. A total of 117 semi-engorged adult H. lusitanicum ticks were collected from 28 adult red deer (Cervus elaphus) in November 2010, at a site (39.63°N, 7.33°W) in Caceres, Spain. Live ticks were transported to the special pathogens laboratory at Hospital San Pedro–CIBIR in Logrono (northern Spain), classified, and frozen at −80°C. For RNA extraction, specimens were washed in 70% ethanol and then in Milli-Q water (Milli-Q Advantage water system; Millipore Iberica, S.A., Madrid, Spain) that had been autoclaved. Each tick was cut lengthwise; half was used for additional processing and the remainder was stored. Before use, each half was crushed in sterile conditions. RNA was individually extracted by using the RNeasy Mini Kit (QIAGEN, Hilden, Germany) according to the manufacturer’s instructions and frozen at −80°C. The RNA was distributed in 12 pools and retrotranscribed by using the Omniscript RT kit (QIAGEN) according to the manufacturer’s instructions and then frozen at −20°C. Nested PCRs were performed by using specific primers for the small segment of CCHFV as described (9). Negative controls (with template DNA but without primers and with primers and containing water instead of template DNA) were included in all assays. For the second round of PCRs, 2 of 12 pools showed amplicons of the expected size (211 bp). Only 1 amplicon could be sequenced. MEGA5 (www.megasoftware.net) was used to compare the sequence with representative small segment sequences of CCHFV available in GenBank (Figure). (Aligned sequences are available from the authors.) Pools of cDNA were submitted to the Spanish National Center of Microbiology (Madrid), where results were confirmed. The CCHFV sequence we report showed 98% genetic similarity (204/209 bp) with sequences recorded for CCHFV in Mauritania and Senegal, on the western coast of Africa. Figure Evolutionary relationships of Crimean-Congo hemorrhagic fever virus strains from Spain and other representative sites. Evolutionary history was inferred by using the unweighted pair group method with arithmetic mean. The optimal tree is shown (sum of ... This finding suggests the circulation of CCHFV in southwestern Europe. The close affinity of the strain from Spain with strains circulating in western Africa and the lack of similarity with isolates from eastern Europe suggest the introduction of this virus from nearby countries of northern Africa. Migratory movements of birds could explain the presence of the virus in southwestern Europe because birds are common hosts of immature H. marginatum, which was reportedly introduced into Europe through annual migratory flights along the western coast of Africa (10). Because of the lack of genetic similarities among virus strains, trade movements of domestic or wild ungulates from eastern Europe do not support our finding. We cannot state whether this virus was circulating previously or if other strains are present in the area because CCHFV detection in the western Mediterranean region has not been previously addressed. H. lusitanicum ticks exist as relatively isolated populations in a narrow strip from Sicily to Portugal. The Mediterranean rabbit and ungulates, the main hosts for immature and adult H. lusitanicum ticks, respectively, are residents of the collection area; however, the movement of these animals through trade has not occurred for several years. Thus, H. lusitanicum ticks could not serve as a spreading vector in the western Mediterranean region. The CCHFV strain from southwestern Europe has been found in ticks restricted to hosts that cannot spread long distances. Therefore, although it would be unlikely, given the strain’s similarity with CCHFV isolates from Senegal and Mauritania, we should not exclude the possibility of an ancient existence for this strain. Additional data collected in the Mediterranean Basin are necessary to establish the actual range of CCHFV.

Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Koch, 1844 (Acari: Ixodidae): hosts, distribution and 16S rDNA sequences

DNA sequences of Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Koch, 1844 were obtained to determine genetic differences between these tick species. Collections of these species are discussed in relation to distribution and hosts. Seven ticks collections (four from Brazil, one from Argentina, one from Uruguay and one from USA) house a total of 1272 A. aureolatum (224 males, 251 females, 223 nymphs and 574 larvae) and 1164 A. ovale (535 males, 556 females, 66 nymphs and 7 larvae). The length of the sequenced mitochondrial 16S rRNA gene fragment for A. aureolatum was 370bp and for A. ovale was 373bp. The DNA sequence analysis showed a 13.1% difference between the two species. Apart from one male A. ovale found on a toad, all adult ticks were found on mammals. The majority of adult specimens of both tick species were removed from Carnivora (96.1 and 84.3% of A. aureolatum and A. ovale, respectively), especially from dogs (53.1% of A. aureolatum, and 46.4% of A. ovale). Collections on wild Canidae were higher for A. aureolatum (23.3%) than for A. ovale (7.1%). On the other hand, collections of A. ovale adults on wild Felidae were higher (18.3%) than findings of A. aureolatum (9.2%). The contribution of other mammalian orders as hosts for adults of A. aureolatum and A. ovale was irrelevant, with the exception of Perissodactyla because Tapiridae contributed with 13.0% of the total number of A. ovale adults. Adults of both tick species have been found occasionally on domestic hosts (apart of the dog) and humans. Most immature stages of A. aureolatum were found on Passeriformes birds, while rodents and carnivores were the most common hosts for nymphs and larvae of A. ovale. A. aureolatum has been found restricted to the Neotropical region, covering the eastern area of South America from Uruguay to Surinam, including northeastern Argentina, eastern Paraguay, southeastern Brazil and French Guiana. A. ovale showed a distribution that covers the Neotropical region from central-northern Argentina throughout the Neotropics into the Nearctic region of Mexico with a few records from the USA, also with collection sites in Paraguay, Bolivia, most Brazilian states, Peru, Ecuador, French Guiana, Surinam, Guyana, Trinidad & Tobago, Venezuela, Colombia, Panama, Costa Rica, Nicaragua, Belize, Guatemala and several states of Mexico.