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Article

Identification and Distribution of Human-Biting Ticks in Northwestern Spain

1
Infectious and Tropical Diseases Research Group (e-INTRO), Biomedical Research Institute of Salamanca-Research Centre for Tropical Diseases at the University of Salamanca (IBSAL-CIETUS), Faculty of Pharmacy, University of Salamanca, 37008 Salamanca, Spain
2
Infectious Diseases Unit, Department of Internal Medicine, University Hospital of Salamanca, 37008 Salamanca, Spain
3
Internal Medicine Department, Ensemble Hospitalier de la Côte, 1110 Morges, Switzerland
4
National Centre for Tropical Medicine, Health Institute Carlos III (ISCIII), 28029 Madrid, Spain
5
Consejería de Sanidad Junta Castilla y León, 47007 Valladolid, Spain
*
Authors to whom correspondence should be addressed.
Academic Editors: Kirby C. Stafford III, Scott C. Williams and Megan A. Linske
Insects 2022, 13(5), 469; https://doi.org/10.3390/insects13050469
Received: 21 March 2022 / Revised: 5 May 2022 / Accepted: 13 May 2022 / Published: 18 May 2022
(This article belongs to the Special Issue Ecology of Ticks and Their Control)
We conducted a tick surveillance study in northwestern Spain. Nymphs of Ixodes ricinus were the most frequently collected. Rhipicephalus bursa, Rhipicephalus sanguineus sensu lato (s.l.), Hyalomma marginatum, Hy. lusitanicum, Dermacentor marginatus, D. reticulatus and Haemaphysalis punctata were also found, with adults as the main stage. The number of collected Hyalomma spp. and R. bursa has been progressively increasing over time. Although bites occurred throughout the year, the highest number of incidents was reported from April to July. The distribution patterns of the tick species were different between the north and the south of the region, which was related to cases detected in humans of the pathogens they carried. Adult men were more likely to be bitten by ticks than women. Ticks were most frequently removed from adults from the lower limbs, while for children, they were mainly attached to the head. Epidemiological surveillance is essential given the increase in tick populations in recent years.

Abstract

Ticks transmit a wide diversity of pathogens to a great variety of hosts, including humans. We conducted a tick surveillance study in northwestern Spain between 2014 and 2019. Ticks were removed from people and identified. Tick numbers, species, development stages, the timeline, seasonal and geographical distribution and epidemiological characteristics of people bitten by ticks were studied. We collected ticks from 8143 people. Nymphs of I. ricinus were the most frequently collected. Rhipicephalus bursa, R. sanguineus s.l., Hy. marginatum, Hy. lusitanicum, D. marginatus, D. reticulatus and H. punctata were also found, with adults as the main stage. The number of collected Hyalomma spp. and R. bursa has been progressively increasing over time. Although bites occurred throughout the year, the highest number of incidents was reported from April to July. The distribution patterns of the tick species were different between the north and the south of the region, which was related to cases detected in humans of the pathogens they carried. Adult men were more likely to be bitten by ticks than women. Ticks were most frequently removed from adults from the lower limbs, while for children, they were mainly attached to the head. Epidemiological surveillance is essential given the increase in tick populations in recent years, mainly of species potentially carrying pathogens causing emerging diseases in Spain, such as Crimean–Congo hemorrhagic fever (CCFH).
Keywords: tick bites; Ixodidae; epidemiology: emerging diseases; Spain tick bites; Ixodidae; epidemiology: emerging diseases; Spain

1. Introduction

Ticks are hematophagous parasites distributed worldwide, and they are of great importance from an epidemiological and clinical point of view. They can transmit a wide variety of pathogens, such as viruses, bacteria and protozoa [1]. Furthermore, they have a great impact in the veterinary field due to economic losses caused by morbidity and mortality, affecting 80% of the world’s cattle population [2], with the total cost of tick-borne diseases (TBDs) estimated to be between USD 14 and 19 billion globally per year [3]. Tick-borne diseases are a growing public health concern, and their incidence is clearly rising worldwide—just look at the increase in the USA of Lyme and human ehrlichiosis and of tick-borne encephalitis (TBE) and hemorrhagic fever cases in Europe and Asia [4]—due to several interacting factors [5,6]. The ecological characteristics of these vectors affect their epidemiology, with their activity cycles closely related to environmental factors such as temperature and relative humidity that are fundamental for their survival. Climate change and weather variability are just two of the many factors that determine tick population abundance, but there are also other variables of importance, such as composition, host community abundance and landscape features [7,8,9].
Ticks from 896 species are known around the world, and the most prevalent Ixodidae family comprises 702 species in 14 genera. Moreover, ixodid ticks are the main vectors of zoonotic pathogens in Europe [10], where 5 genera (Ixodes, Dermacentor, Haemaphysalis, Rhipicephalus and Hyalomma) and 54 species have been found, with I. ricinus being the most widely distributed tick [9,11,12]. Lyme borreliosis is the most prevalent tick-borne disease in Europe, and it is caused by Borrelia burgdorferi sensu lato (s.l.) complex [13]. In the Iberian Peninsula, there are five genera of ixodid ticks that bite humans: Ixodes, Dermacentor, Rhipicephalus, Haemaphysalis and Hyalomma, which are potential transmitters of B. burgdorferi sensu lato, several genospecies of Rickettsia, Anaplasma phagocytophilum and the Crimean–Congo virus [14].
The association between global warming and the emergence of TBDs is well documented in Europe and Eurasia [15]. The geographical expansion of tick species is directly related to the emergence of new infectious diseases, which makes it more necessary than ever to understand the dynamics and distribution of ticks. Although there is much previous information about the distribution of ticks in several areas of Spain, the data come mainly from the study of captured ticks in the environment, either from vegetation or animals (wild and domestic) [9,16,17,18,19,20]. The region of Castilla y León is characterized by a great diversity of tick species, as we find both those typical of humid climates and those of Mediterranean climates. There is a very exhaustive study of ticks removed from people in Castilla y León carried out by our group [14] in the period corresponding to 1997–2002. Data on the species collected from humans in this study showed that in the north, I. ricinus was the dominant species, followed by both species of Dermacentor and H. punctata. In the south, in addition to the species mentioned above (except D. reticulatus) we found R. bursa, Hy. marginatum and R. sanguineus, which were very abundant in zones rich in livestock and dogs. Although some species are active all year round, most of them are most active in spring–early summer (April–July) and autumn. A long time has passed since then, and given the emergence of new species of ticks and the introduction of new TBDs, such as Crimean–Congo hemorrhagic fever (CCHF) and DEBONEL (Dermacentor-borne necrosis erythema and lymphadenopathy), it seems essential to re-examine the current situation in this area of Spain. Thus, the purpose of this work is to update data about species of ticks removed from people and their spatial and temporal patterns. This will allow identifying the risk areas, activity peaks and dynamics of these vectors.

2. Materials and Methods

2.1. Study Site/Site Selection

This study was performed in Castilla y León (41°23′0″ N, 4°27′0″ W), an area located in northwestern Spain. It covers a surface of 94,224 km2 and is one of the most extensive regions of the European Union. Although there is a marked continental climate in most of the territory, characterized by cold winters and hot summers with short periods of spring and autumn, regional variations in both temperatures and rainfall allow us to distinguish different climatic domains in the region: continentalized Mediterranean in the center, with semi-arid enclaves in some areas, mountain Mediterranean in mountainous areas in the northeast, east and south and Atlantic in the north (Figure 1). This great geomorphological and bioclimatic variety, together with its vast extension, gives rise to a great range of climatological conditions and ecosystems which undoubtedly affects the geographical distribution of the different tick species. Castilla y León is rich in forests and ample wooded areas, and the privileged geographical situation of the northern subplateau makes it a region of special interest as an area of passage, breeding and wintering of birds from Central and Northern Europe and the African continent.

2.2. Tick Collection and Identification

During 2014–2019, ticks were collected from people who went to primary healthcare centers and hospital emergency services in Castilla y León for their removal through a program of the Junta de Castilla y León for the prevention and control of tick-borne anthropozoonoses. The ticks were removed from the hosts with tweezers and sent to our laboratory (Laboratory of the Faculty of Pharmacy at the University of Salamanca) at room temperature in a container. Each tick was morphologically identified under a binocular lens in terms of life stage and species using taxonomic reference keys [9,21,22,23]. Each tick was identified to the species level, except in the case of R. sanguineus (s.l.) ticks, which were identified only to the “group” level as the re-definition of R. sanguineus sensu stricto (s.s.) [24] was not available during most of the study. Rhipicephalus turanicus specimens were also reported as R. sanguineus s.l. Tick species, developmental stages (larva, nymph, adult), sex and feeding degree were recorded, as well as the epidemiological characteristics of the patients (age, sex, geographical location) and anatomic location of the attachment of the tick on the patient. A unique individual identification number was assigned to each tick and its corresponding file.

2.3. Geopositioning and Data Analysis

Information about tick bites was obtained from the database of the center of reference of the Biomedical Research Institute of Salamanca-Research Center for Tropical Diseases at the University of Salamanca. To obtain the geographical coordinates of every tick bite, we geocoded the locations of tick collections using “Batch geocoder for journalists” (https://geocode.localfocus.nl, accessed on 28 February 2022), prior to data curation. The latitude and longitude were then projected to the coordinate reference system ETRS89 to map the distribution of the species of interest through the years and the median temperature in the provinces of the autonomous community of Castilla y León, using pretty breaks as a data classification method. All the maps were constructed in QGIS 3.18.3 “Zürich” (Open Source Geospatial Foundation) [25].
Absolute frequencies were used to summarize the number of each species and show visual tendencies across years and seasons. Relative frequencies converted into percentages were used to visualize tendencies between the sex and life stages of the collected ticks, and both frequencies were used to show the epidemiological characteristics of people bitten by ticks.
In addition, we searched for signals of displacement in the geographic distribution of the collected ticks. For the visual pattern, we used geographic coordinates of the previous geocode step. The comparative figures were constructed using the package ggplot2 [26], in the statistical environment R [27]. The Kruskal–Wallis rank sum test and pairwise comparisons using the Wilcoxon rank sum test with continuity correction were used for statistical support in R. Chi-square analysis was conducted to evaluate differences in sex specimens. Values of p were adjusted using the false discovery rate and Bonferroni methods, considering values less than or equal to 0.05 as statistically significant.

3. Results

3.1. Tick Numbers, Species, Development Stages and Timeline

A total of 8143 ticks were collected over 6 years, of which 8081 were identified to the species level and life stage (larva, nymph and adult). The remaining 62 were discarded as their morphological identification was impossible due to the structural and conservation state in which they were received. Ixodid ticks belonging to five genera and eight species were found (Table 1); I. ricinus was the most frequent species infesting humans (52.29%), followed by R. bursa (12.15%), R. sanguineus s.l. (10.38%), Hy. marginatum (9.08%), D. marginatus (8.06%), Hy. lusitanicum (3.79%), D. reticulatus (2.48%) and H. punctata (1.73%). Although this general trend was maintained over the six years of the study, during recent years, there has been a clear increase in Hy. lusitanicum and Rhipicephalus bursa.
Regarding the temporal distribution (Figure 2), while some species remained stable over time (D. reticulatus and H. punctata), others underwent changes. Hyalomma lusitanicum is a clear example of how a species has increased over time (linear model, R2 = 0.9216, F-statistic p < 0.05), especially since 2015. Similarly, this occurred with R. bursa, with a huge growth spike in 2019 (linear model, R2 = 0.6188, F-statistic p < 0.05). Dermacentor marginatus and Hy. marginatum had roughly identical temporal distributions with clear downward trends in 2017 and 2018 before recovering in 2019. Rhipicephalus sanguineus and I. ricinus both had their maximum peak in 2015. Despite this, both species exhibited a downward trend.
The adult stage (male and female) was the most frequent in all genera (Figure 3) except for Ixodes, where nymphs (60.31%) were collected in much larger numbers (Table 1). For Dermacentor, Haemaphysalis and Rhipicephalus, we observed a higher percentage of females compared to males and nymphs (64.24%, 57.85% and 56.72%, respectively) for all the species, while for Hyalomma species, the adults recovered were mainly males (68.20%). Larvae were recovered only from I. ricinus. This composition of females and males did not change throughout the study.

3.2. Seasonal and Geographical Distribution of Ticks

The highest number of tick bites (78%, n = 6303) was reported during spring and summer (April to July) and the lowest in winter (January and early February) (8.90%, n = 719). Ixodes ticks were the most frequent and widely distributed species (Figure 4), and although they were detected throughout the year, their highest detection levels were in spring, autumn and early winter for the adult stage and spring and summer for the nymphs (June mainly). Adult stages of the genus Hyalomma were removed throughout the year, although very sporadically in winter and autumn, with peak activity in spring and early summer for both species (June and July). Rhipicephalus had one activity peak in spring with a decrease in summer (most bites in May and June) and practically disappeared in autumn and winter in the case of R. bursa. For R. sanguineus, despite the decreases in the number of cases, it was still active during these seasons. Both species of Dermacentor were active all year, although they showed pronounced seasonality with two annual peaks of maximum activity in spring and autumn for D. marginatus and autumn and winter for D. reticulatus, with very little or no presence in summer. Most D. marginatum bites were in April and May, with slightly lower peaks in October and March, while most bites by D. reticulatus occurred in December and March, with a smaller peak in April. Haemaphysalis had a very low occurrence and was limited to spring (May and June).
Ixodes ricinus was the species more frequently removed from persons in all seasons. When analyzing the behavior of the remaining species, we observed that R. sanguineus and R. bursa were the most frequent ticks removed in spring, Hy. marginatum and R. bursa in summer and D. marginatus and D. reticulatus in autumn and winter.
The geographical distribution showed variations among the different species of ticks (Figure 5).
Almost all ticks were removed from all provinces of the community except for D. reticulatus and H. punctata. Ixodes ricinus showed a higher prevalence in the northeast, and both Dermacentor species in the northern areas, while Hyalommma spp. were detected mainly in the south. Rhipicephalus spp. showed differences in the distribution of the species, and R. bursa was mainly distributed in the south, while R. sanguineus was mainly distributed in the south and the northeast. Haemaphysalis was the less represented genus, mostly found in the northeast, with little or no presence in the other areas.
Looking at how the distribution of ticks has varied over the years by analyzing the latitude and longitude (Figure 6), we can see there was a tendency to move northwards and westwards when analyzing the data as a group. In the case of the longitude, this was statistically significant both at the group level (χ2: 19.422, df = 5, p < 0.05) and by year: 2018 compared with 2015 (Z: −3.175819; p-adjusted fdr < 0.05), 2019 compared with 2014 (Z: −2.879612; p-adjusted fdr < 0.05) and 2019 compared with 2015 (Z: −3.613219; p-adjusted fdr < 0.05). In the case of the latitude, this was statistically significant only at the group level (χ2: 13.895, df = 5, p < 0.05).

3.3. Epidemiological Characteristics of People Bitten by Ticks

Data on sex, age and sites of tick bites on people are shown in Table 2. Epidemiological characteristics of the patients were available for 6732 ticks regarding sex, 6460 regarding children/adults and 5736 for age classes. According to the sex of people bitten by ticks, 65.40% were men and 34.59% were women. Ticks were collected from people of all ages: 22.59% of those bitten were children (<14 years), and the remaining 77.39% were adults. The lowest number of bites was found in the 15–35 age group (16.94%). In contrast, the group most frequently bitten by ticks was the 55+ age group (32.98%).
Using the chi-square test (χ2 = 339.90, df = 21, p < 0.05), we observed statistically significant differences between age groups for each of the species, except in the case of D. reticulatus. We removed the greatest number of ticks from the species I. ricinus, R. bursa, D. marginatus, Hy. marginatum and Hy. lusitanicum from the 55+ age group, while R. sanguineus and H. punctata were mostly retired from the children’s age group (0–14).
We observed that for all species, the number of ticks removed from men was significantly higher than from women, except in the case of H. punctata, in which the number of ticks recovered from women was higher. There were statistically significant differences (χ2 = 226.67, df = 7, p < 0.05).
Ticks were most frequently removed from adults from the lower limbs (29.12% of 3561), and children were mainly bitten on the head (38.25% of 1422). Ixodes ricinus and Hyalomma spp. were removed more frequently from the lower limbs than from other body locations, while R. sanguineus., Dermacentor spp. and H. punctata were mainly fixed on the head. In the case of ticks belonging to the R. bursa species, the main attachment site was the thorax.

4. Discussion

The emergence of novel tick-borne diseases in recent years has made it essential to understand the distribution of tick populations. Although there are already studies on the distribution of ticks in different areas of Spain [6,14,16,17,18,19,28,29], data on tick species, their distribution and activity have probably undergone changes in recent years. The present study provides epidemiological information on the diversity, relative abundance and seasonal and geographic distribution of human-biting ticks in Castilla y León (northwest Spain) over a six-year span (2014–2019), allowing us to understand tick activity and the periods of highest risk to humans.
Ixodes ricinus was the most predominant and widely distributed species, both spatially and temporally, with a clear dominance over the others, followed by R. bursa. These results coincide with those observed in other studies carried out by our group seventeen years ago [14], in which I. ricinus and R. bursa were also the prevalent species. However, data about other ticks have changed over the years. Hyalomma marginatum is currently the fourth most frequently removed species from humans, followed very closely by R. sanguineus s.l, whereas in a previous study (1996–2002), it was ranked fifth behind D. marginatus. Nevertheless, the percentage of recovered ticks belonging to D. marginatus was higher in the 1997–2002 period. The most evident case of a change in distribution patterns and abundance was found for Hy. lusitanicum, which currently accounts for 4.2% of the ticks removed from humans, compared to 0.85% in the previous study. In this sense, keep in mind that ticks of the genus Hyalomma are the main vectors of CCHFV, which is currently considered an emerging or possibly a re-emerging pathogen in Southern Europe. Although the presence of this virus was already reported in Spain in 2010 [30], an increase in human CCHFV cases in Spain and, more specifically, in Castilla y León has been detected, as reported by our group [31,32]. The increase in human cases matched the increase in Hyalomma ticks observed in this area. All observed changes in both distribution patterns and frequency of ticks are determined not only by biotic factors such as climate or abiotic factors (vegetation), but also by the accessibility of hosts.
The predominance of I. ricinus over the other species is not unique to the study area. The same pattern has been observed in studies carried out in different locations in Spain [14,18,29,33,34,35] and in European countries such as Belgium, Italy, Sweden, the Netherlands, the United Kingdom, Finland, Norway, Romania and Germany. The nymph is the predominant stage of I. ricinus, which is also consistent with what was observed in a study previously conducted by our group [14]. Our results compared with those obtained across Europe are lower than those reported in Belgium and Great Britain, higher than those in Italy and similar to those in Sweden [36,37].
Although we cannot conclude that ticks have a preference among human hosts according to their sex, of the 7862 participants included in this study, 65.40% were men and 34.59% were women. This preference for males is very similar to that observed by Fernández Soto in 2003 (62% men and 38% women). The fact that this pattern remains the same as it was almost 20 years ago may indicate that the occupational and behavioral habits in terms of outdoor activities among men and women have not changed. Thus, 22.59% of tick bite victims are in the age group of 14 years old or younger, while the 15–35 group has the lowest number of tick bites at 16.94%, in line with Northern Europe [38] and Belgium [36].
Differences in anatomical sites of attachment were observed for both children and adults. Tick bites occurred most frequently on the lower limbs and thorax in adults and on the head in children. Similar results have been observed in other studies in Western and Northern Europe, with a predominance of bites on the legs in adults and the head and neck in children [13,38,39,40,41]. These apparent preferences, as suggested by some authors, are probably due to the morphological, behavioral and physiological differences between men and women and adults and children. Adult legs and children’s heads are the most accessible places for ticks since they are at the height of the vegetation where ticks search for a host.
Although ticks are removed during all months of the year, the highest number of tick bites are recorded during spring and summer, with a peak of tick activity in June and July, as observed in this same area in previous studies. These data are also in accordance with several studies carried out in Europe [13,38,39,40,42,43,44]. When looking at the temporal distribution of the different genera, we observed that adults of Ixodes were detected throughout the year but mostly in spring, autumn and later winter (March), which differed somewhat from previous years in the same study area where adults were biting mainly in autumn and spring but not in winter [14]. These activity patterns are similar to those in several countries of Northern Europe [13,36,42,45]. Hyalomma is infrequent in winter, with its peak activity in spring and summer, with June and July being the months with the most reported cases for both species. In recent years, we have seen that Hy. marginatum bites are being brought forward to May. The activity pattern of Rhipicephalus has been maintained in northwestern Spain over time, with two peaks in spring and summer, although as with Hyalomma, in the case of R. bursa, there are many reports of bites as early as May. Dermacentor shows a particular seasonality, being practically absent in summer for both species, which could lead us to think that it does not feel comfortable with hot temperatures. Dermacentor marginatus presents a bimodal activity pattern with peaks in spring (April–May) and autumn, and the peak number of bites always in April. In the case of D. reticulatus, bites occur similarly in autumn, winter and spring (from October to March). This differs from the situation observed in Belgium, where the highest peaks of activity occur in spring (March–May) and late summer and autumn (August–November) [36]. Haemaphysalis is practically limited to spring. Although previous studies have reported cases in summer, we have not seen them.
While studying the geographical distribution of the ticks, we observed quite stable and different distribution patterns between the north and the south. These distribution patterns were determined by various climatic (temperature and humidity) and ecological factors. Dermacentor marginatus, D. reticulatus and H. punctata were mainly distributed in the north of the study area, although the greatest increase in D. marginatus was seen in the southwest. On the other hand, Hy. marginatum, Hy. lusitanicum and R. bursa were found in greater numbers in the south. Hyalomma marginatum is expanding its habitat to southwestern areas, and Hy. lusitanicum in recent years to arid or semi-arid areas in the west. The wider distribution of Hyalomma in the south could explain the increasing occurrence of CCFH virus observed in this area in recent years. Finally, I. ricinus and R. sanguineus were distributed in both areas. However, the greatest number of specimens was found in the northeast for both, especially I. ricinus.

5. Conclusions

Our results show that humans from northwestern Spain are mainly bitten by I. ricinus nymphs. Ticks bite particularly on the legs of adults and on the head of children. Therefore, although the peak season for tick bites is spring and summer, tick bites are becoming increasingly frequent in autumn and even winter. Seasonal tick patterns have changed in recent years, both in Spain and elsewhere in Europe, where many species of ticks have expanded their distribution. The increased period of activity increases the likelihood of being bitten and therefore of being infected by a tick-borne pathogen. This study is essential for proper epidemiological surveillance. Moreover, knowledge of tick populations and human exposure to tick bites could suggest ways to reduce the risk of tick-borne diseases.

Author Contributions

Conceptualization, A.M., M.B.-G., M.B.V.S. and M.C.V.L.; methodology, Z.H., A.B. and M.C.V.L.; software, C.P.P.; formal analysis, J.S.-M., L.C.M.A. and J.D.S.L.; investigation, M.C.V.L.; data curation, M.C.V.L.; writing—original draft preparation, A.M., M.B.V.S., M.B.-G. and M.C.V.L.; writing—review and editing, A.M., M.B.-G., M.B.V.S., J.D.S.L., J.S.-M. and M.C.V.L.; visualization, M.C.V.L.; supervision, A.M., M.B.-G. and M.B.V.S.; project administration, A.M., M.B.-G., M.B.V.S. and M.C.V.L.; funding acquisition, R.d.Á.-S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Junta de Castilla y León. Consejería de Sanidad.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available within the article.

Acknowledgments

We want to thank the Junta de Castilla y León.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Estrada-Peña, A.; Jongejan, F. Ticks feeding on humans: A review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp. Appl. Acarol. 1999, 23, 685–715. [Google Scholar] [CrossRef] [PubMed]
  2. Yitayew, D.; Samuel, D. Tick borne hemoparasitic diseases of ruminants: A review. Adv. Biol. Res. 2015, 9, 210–224. [Google Scholar] [CrossRef]
  3. Ghosh, S.; Azhahianambi, P.; Yadav, M.P. Upcoming and future strategies of tick control: A review. J. Vector Borne Dis. 2007, 44, 79–89. [Google Scholar] [PubMed]
  4. Rochlin, I.; Toledo, A. Emerging tick-borne pathogens of public health importance: A mini-review. J. Med. Microbiol. 2020, 69, 781–791. [Google Scholar] [CrossRef]
  5. Dantas-Torres, F.; Chomel, B.B.; Otranto, D. Ticks and tick-borne diseases: A One Health perspective. Trends Parasitol. 2012, 28, 437–446. [Google Scholar] [CrossRef]
  6. Estrada-Peña, A.; de la Fuente, J.; Cabezas-Cruz, A. Functional redundancy and ecological innovation shape the circulation of tick-transmitted pathogens. Front. Cell. Infect. Microbiol. 2017, 7, 234. [Google Scholar] [CrossRef]
  7. Gortazar, C.; Reperant, L.A.; Kuiken, T.; de la Fuente, J.; Boadella, M.; Martínez-Lopez, B.; Ruiz-Fons, F.; Estrada-Peña, A.; Drosten, C.; Medley, G.; et al. Crossing the Interspecies Barrier: Opening the Door to Zoonotic Pathogens. PLoS Pathog. 2014, 10, e1004129. [Google Scholar] [CrossRef][Green Version]
  8. Estrada-Peña, A.; De La Fuente, J. The ecology of ticks and epidemiology of tick-borne viral diseases. Antivir. Res. 2014, 108, 104–128. [Google Scholar] [CrossRef]
  9. Estrada-Peña, A.; Martinez, J.M.; Sanchez Acedo, C.; Quilez, J.; Del Cacho, E. Phenology of the tick, Ixodes ricinus, in its southern distribution range (central Spain). Med. Vet. Entomol. 2004, 18, 387–397. [Google Scholar] [CrossRef]
  10. Gilbert, L. Altitudinal patterns of tick and host abundance: A potential role for climate change in regulating tick-borne diseases? Oecologia 2010, 162, 217–225. [Google Scholar] [CrossRef]
  11. Rizzoli, A.; Silaghi, C.; Obiegala, A.; Rudolf, I.; Hubálek, Z.; Földvári, G.; Plantard, O.; Vayssier-Taussat, M.; Bonnet, S.; Špitalská, E.; et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: New hazards and relevance for public health. Front. Public Health 2014, 2, 251. [Google Scholar] [CrossRef] [PubMed]
  12. Boulanger, N.; Boyer, P.; Talagrand-Reboul, E.; Hansmann, Y. Ticks and tick-borne diseases. Med. Mal. Infect. 2019, 49, 87–97. [Google Scholar] [CrossRef] [PubMed]
  13. Cull, B.; Pietzsch, M.E.; Gillingham, E.L.; McGinley, L.; Medlock, J.M.; Hansford, K.M. Seasonality and anatomical location of human tick bites in the United Kingdom. Zoonoses Public Health 2019, 67, 112–121. [Google Scholar] [CrossRef]
  14. Fernández-Soto, P. Garrapatas que Parasitan a Personas en Castilla y León, Determinación por Serología de su Parasitismo y Detección Molecular de los Patógenos que Albergan; Universidad de Salamanca: Salamanca, Spain, 2003. [Google Scholar]
  15. El-Sayed, A.; Kamel, M. Climatic changes and their role in emergence and re-emergence of diseases. Environ. Sci. Pollut. Res. 2020, 27, 22336–22352. [Google Scholar] [CrossRef] [PubMed]
  16. Barandika, J.F.; Hurtado, A.; García-Sanmartín, J.; Juste, R.A.; Anda, P.; García-Pérez, A.L. Prevalence of tick-borne zoonotic bacteria in questing adult ticks from Northern Spain. Vector-Borne Zoonotic Dis. 2008, 8, 829–835. [Google Scholar] [CrossRef] [PubMed]
  17. Fernández de Mera, I.G.; Ruiz-Fons, F.; de la Fuente, G.; Mangold, A.J.; Gortázar, C.; de la Fuente, J. Spotted fever group rickettsiaein questing ticks, central Spain. Emerg. Infect. Dis. 2013, 19, 1163–1165. [Google Scholar] [CrossRef][Green Version]
  18. Requena-García, F.; Cabrero-Sañudo, F.; Olmeda-García, S.; González, J.; Valcárcel, F. Influence of environmental temperature and humidity on questing ticks in central Spain. Exp. Appl. Acarol. 2017, 71, 277–290. [Google Scholar] [CrossRef]
  19. Remesar, S.; Fernández, P.D.; Venzal, J.M.; Pérez-Creo, A.; Prieto, A.; Estrada-Peña, A.; López, C.M.; Panadero, R.; Fernández, G.; Díez-Baños, P.; et al. Tick species diversity and population dynamics of Ixodes ricinus in Galicia (north-western Spain). Ticks Tick. Borne. Dis. 2019, 10, 132–137. [Google Scholar] [CrossRef]
  20. Estrada-Peña, A.; Roura, X.; Sainz, A.; Miró, G.; Solano-Gallego, L. Species of ticks and carried pathogens in owned dogs in Spain: Results of a one-year national survey. Ticks Tick. Borne. Dis. 2017, 8, 443–452. [Google Scholar] [CrossRef]
  21. Gil-Collado, J.; Guillén, J.L.; Zapatero, L.M. Claves para la identificación de los Ixodoidea españoles (adultos). Rev. Ibérica Parasitol. 1979, 39, 107–118. [Google Scholar]
  22. Estrada-Peña, A.; Mihalca, A.D.; Petney, T.N. Ticks of Europe and North Africa: A Guide to Species Identification; Springer International Publishing: Cham, Switzerland, 2017; ISBN 9783319637594. [Google Scholar]
  23. Apanaskevich, D.A.; Santos-Silva, M.M.; Horak, I.G. The genus Hyalomma Koch, 1844. IV. Redescription of all parasitic stages of H. (Euhyalomma) lusitanicum Koch, 1844 and the adults of H. (E.) franchinii Tonelli Rondelli, 1932 (Acari: Ixodidae) with a first description of its immature stages. Folia Parasitol. 2008, 55, 61–74. [Google Scholar] [CrossRef] [PubMed][Green Version]
  24. Nava, S.; Beati, L.; Venzal, J.M.; Labruna, M.B.; Szabó, M.P.J.; Petney, T.; Saracho-Bottero, M.N.; Tarragona, E.L.; Dantas-Torres, F.; Silva, M.M.S.; et al. Rhipicephalus sanguineus (Latreille, 1806): Neotype designation, morphological re-description of all parasitic stages and molecular characterization. Ticks Tick. Borne. Dis. 2018, 9, 1573–1585. [Google Scholar] [CrossRef] [PubMed]
  25. QGIS.org. QGIS Geographic Information System; QGIS Association: Geneva, Switzerland, 2022. [Google Scholar]
  26. Wickham, H. Ggplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2016. [Google Scholar]
  27. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021. [Google Scholar]
  28. Merino, F.J.; Nebreda, T.; Serrano, J.L.; Fernández-Soto, P.; Encinas, A.; Pérez-Sánchez, R. Tick species and tick-borne infections identified in population from a rural area of Spain. Epidemiol. Infect. 2005, 133, 943–949. [Google Scholar] [CrossRef] [PubMed]
  29. Fernández-Soto, P.; Pérez-Sánchez, R.; Álamo-Sanz, R.; Encinas-Grandes, A. Spotted fever group rickettsiae in ticks feeding on humans in northwestern Spain: Is Rickettsia conorii vanishing? Ann. N. Y. Acad. Sci. 2006, 1078, 331–333. [Google Scholar] [CrossRef] [PubMed]
  30. Estrada-Peña, A.; Palomar, A.M.; Santibáñez, P.; Sánchez, N.; Habela, M.A.; Portillo, A.; Romero, L.; Oteo, J.A. Crimean-Congo Hemorrhagic Fever Virus in Ticks, Southwestern Europe, 2010. Emerg. Infect. Dis. 2012, 18, 179–180. [Google Scholar] [CrossRef] [PubMed]
  31. Monsalve Arteaga, L.; Muñoz Bellido, J.L.; Negredo, A.I.; García Criado, J.; Vieira Lista, M.C.; Sánchez Serrano, J.Á.; Vicente Santiago, M.B.; López Bernús, A.; de Ory Manchón, F.; Sánchez Seco, M.P.; et al. New circulation of genotype V of Crimean-Congo haemorrhagic fever virus in humans from Spain. PLoS Negl. Trop. Dis. 2021, 15, e0009197. [Google Scholar] [CrossRef]
  32. Monsalve-Arteaga, L.; Alonso-Sardón, M.; Muñoz Bellido, J.L.; Vicente Santiago, M.B.; Vieira Lista, M.C.; López Abán, J.; Muro, A.; Belhassen-García, M. Seroprevalence of Crimean-Congo hemorrhagic fever in humans in the World Health Organization European region: A systematic review. PLoS Negl. Trop. Dis. 2020, 14, e0008094. [Google Scholar] [CrossRef]
  33. Espí, A.; Del Cerro, A.; Somoano, A.; García, V.; Prieto, J.M.; Barandika, J.F.; García-Pérez, A.L. Borrelia burgdorferi sensu lato prevalence and diversity in ticks and small mammals in a Lyme borreliosis endemic Nature Reserve in North-Western Spain. Incidence in surrounding human populations. Enferm. Infecc. Microbiol. Clin. (Engl. Ed.) 2017, 35, 563–568. [Google Scholar] [CrossRef]
  34. Barandika, J.F.; Olmeda, S.A.; Casado-Nistal, M.A.; Hurtado, A.; Juste, R.A.; Valcárcel, F.; Anda, P.; García-Pérez, A.L. Differences in questing tick species distribution between Atlantic and continental climate regions in Spain. J. Med. Entomol. 2011, 48, 13–19. [Google Scholar] [CrossRef]
  35. Remesar, S.; Díaz, P.; Portillo, A.; Santibáñez, S.; Prieto, A.; Díaz-Cao, J.M.; López, C.M.; Panadero, R.; Fernández, G.; Díez-Baños, P.; et al. Prevalence and molecular characterization of Rickettsia spp. in questing ticks from north-western Spain. Exp. Appl. Acarol. 2019, 79, 267–278. [Google Scholar] [CrossRef]
  36. Lernout, T.; De Regge, N.; Tersago, K.; Fonville, M.; Suin, V.; Sprong, H. Prevalence of pathogens in ticks collected from humans through citizen science in Belgium. Parasit. Vectors 2019, 12, 550. [Google Scholar] [CrossRef] [PubMed]
  37. Cull, B.; Pietzsch, M.E.; Hansford, K.M.; Gillingham, E.L.; Medlock, J.M. Surveillance of British ticks: An overview of species records, host associations, and new records of Ixodes ricinus distribution. Ticks Tick. Borne. Dis. 2018, 9, 605–614. [Google Scholar] [CrossRef] [PubMed]
  38. Wilhelmsson, P.; Lindblom, P.; Fryland, L.; Nyman, D.; Jaenson, T.G.; Forsberg, P.; Lindgren, P.E. Ixodes ricinus ticks removed from humans in Northern Europe: Seasonal pattern of infestation, attachment sites and duration of feeding. Parasites Vectors 2013, 6, 362. [Google Scholar] [CrossRef] [PubMed]
  39. Hügli, D.; Moret, J.; Rais, O.; Moosmann, Y.; Erard, P.; Malinverni, R.; Gern, L. Tick bites in a Lyme borreliosis highly endemic area in Switzerland. Int. J. Med. Microbiol. 2009, 299, 155–160. [Google Scholar] [CrossRef] [PubMed][Green Version]
  40. Robertson, J.N.; Gray, J.S.; Stewart, P. Tick bite and Lyme borreliosis risk at a recreational site in England. Eur. J. Epidemiol. 2000, 16, 647–652. [Google Scholar] [CrossRef] [PubMed]
  41. Pańczuk, A.; Tokarska-Rodak, M.; Mikuľáková, W.; Kendrová, L.; Magurová, D. Exposure to ticks and undertaking lyme borreliosisprevention activities among students from Poland and Slovakia. Ann. Agric. Environ. Med. 2019, 26, 217–221. [Google Scholar] [CrossRef] [PubMed]
  42. Briciu, V.T.; Titilincu, A.; Ţăţulescu, D.F.; Cârstina, D.; Lefkaditis, M.; Mihalca, A.D. First survey on hard ticks (Ixodidae) collected from humans in Romania: Possible risks for tick-borne diseases. Exp. Appl. Acarol. 2011, 54, 199–204. [Google Scholar] [CrossRef]
  43. Weisshaar, E.; Schaefer, A.; Scheidt, R.R.W.; Bruckner, T.; Apfelbacher, C.J.; Diepgen, T.L. Epidemiology of tick bites and borreliosis in children attending kindergarten or so-called “forest kindergarten” in southwest Germany. J. Investig. Dermatol. 2006, 126, 584–590. [Google Scholar] [CrossRef] [PubMed][Green Version]
  44. Manfredi, M.T.; Dini, V.; Piacenza, S.; Genchi, C. Tick species parasitizing people in an area endemic for tick-borne diseases in north-western Italy. Parassitologia 1999, 41, 555–560. [Google Scholar]
  45. Lindblom, A.; Wallménius, K.; Sjöwall, J.; Fryland, L.; Wilhelmsson, P.; Lindgren, P.E.; Forsberg, P.; Nilsson, K. Prevalence of Rickettsia spp. in ticks and serological and clinical outcomes in tick-bitten individuals in Sweden and on the Åland Islands. PLoS ONE 2016, 11, e0166653. [Google Scholar] [CrossRef][Green Version]
Figure 1. Map of the area of study (Castilla y León, NW Spain). (a) Altitude. (b) Medium annual temperature. Source: Atlas Agroclimático de Castilla y León—ITACYL-AEMET-2013 (http://atlas.itacyl.es, accessed on 24 April 2022).
Figure 1. Map of the area of study (Castilla y León, NW Spain). (a) Altitude. (b) Medium annual temperature. Source: Atlas Agroclimático de Castilla y León—ITACYL-AEMET-2013 (http://atlas.itacyl.es, accessed on 24 April 2022).
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Figure 2. Trends in the number of ticks recovered over time.
Figure 2. Trends in the number of ticks recovered over time.
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Figure 3. Number of tick species according to developmental stages.
Figure 3. Number of tick species according to developmental stages.
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Figure 4. Seasonality of tick bites on humans. (A) I. ricinus. (B) D. marginatus, D. reticulatus, H. punctata, Hy. Lusitanicum, Hy. Marginatum, R. bursa and R. sanguineus. Species sampled by season and year: winter (December–February), spring (March–May), summer (June–August) and autumn (September–November).
Figure 4. Seasonality of tick bites on humans. (A) I. ricinus. (B) D. marginatus, D. reticulatus, H. punctata, Hy. Lusitanicum, Hy. Marginatum, R. bursa and R. sanguineus. Species sampled by season and year: winter (December–February), spring (March–May), summer (June–August) and autumn (September–November).
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Figure 5. Geographical distribution of ticks. Source: QGIS 3.18.3 “Zürich” (Open Source Geospatial Foundation).
Figure 5. Geographical distribution of ticks. Source: QGIS 3.18.3 “Zürich” (Open Source Geospatial Foundation).
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Figure 6. Longitudinal and latitudinal patterns over time.
Figure 6. Longitudinal and latitudinal patterns over time.
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Table 1. Numbers of collected ticks, species, life stages and sex.
Table 1. Numbers of collected ticks, species, life stages and sex.
Tick SpeciesNumbers of Collected Ticks
LarvaeNymphsMaleFemaleTotal
Ixodes ricinus22125491814384226
Rhipicephalus bursa 25406551982
Rhipicephalus sanguineus126330482839
Hyalomma marginatum 2499233734
Dermacentor marginatus 5219428652
Hyalomma lusitanicum 121195307
Dermacentor reticulatus 81120201
Haemaphysalis punctata 35681140
Total2222611182034288081
Table 2. Epidemiological characteristics of people bitten by ticks (2014–2019).
Table 2. Epidemiological characteristics of people bitten by ticks (2014–2019).
Characteristics of PatientsNumbers and Species of Ticks Collected from Patients
I.ricinusR. bursaR. sanguineusD. marginatusD. reticulatusHy. marginatumHy. lusitanicumH. punctataTotal
Sex: men (%)
women (%)
2247 (65.75%)
1170 (34.24%)
633 (73.43%)
229 (26.56%)
411(59.13%)
284 (40.86%)
292 (50.78%)
283 (49.21%)
100 (56.81%)
76 (43.18%)
495 (75.68%)
159 (24.31%)
218 (75.69%)
70 (24.30%)
7 (10.76%)
58 (89.23%)
4403 (65.40%)
2329 (34.59%)
Total3417862695575176654288656732
Age:
0–14673163214126342913441296 (22.59%)
15–355051401085140813512972 (16.94%)
36–558401901011343719261211576 (27.47%)
55+88222814718526269124311892 (32.98%)
Total29007215704961375712331085736
Adults (%)
Children (%)
2478 (75.66%)
797 (24.33%)
615 (75.64%)
198 (24.35%)
408 (60.80%)
263 (39.19%)
403 (73.54%)
145 (26.45%)
124 (75.60%)
40 (24.39%)
580 (94.61%)
33 (5.38%)
240 (93.75%)
16 (6.25%)
70 (58.33%)
50 (41.66%)
4918 (76.13%)
1542 (23.86%)
Total32758136715481646132561206460
Site of bites:Adults/ChildrenAdults/ChildrenAdults/ChildrenAdults/ChildrenAdults/ChildrenAdults/ChildrenAdults/ChildrenAdults/ChildrenAdults/Children
Head42/13254/9474/151182/10228/1917/911/516/32424 (43.80%)/544 (56.19%)
Neck37/5943/1946/3326/813/329/915/56/7215 (60.05%)/143 (39.94%)
Thorax458/159120/2760/2220/79/6100/1950/98/2825 (76.67%)/251 (23.32)
Upper limbs284/7641/1232/1420/412/836/811/26/1442 (77.95%)/125 (22.04%)
Lower limbs681/18898/939/919/517/8125/1952/86/11037 (84.65%)/188 (15.34)
Back149/4746/1531/1114/48/344/821/24/1317 (76.69%)/91 (22.30%)
Pelvis147/4442/1416/54/30/069/818/55/1301 (79%)/80 (20.99%)
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