Next Article in Journal
Megaselia scalaris and Senotainia tricuspis Infesting Apis mellifera: Detection by Quantitative PCR, Genotyping, and Involvement in the Transmission of Microbial Pathogens
Next Article in Special Issue
An Overview of the Thrips Fauna of the “Góra Bucze” Landscape-Nature Complex in Western Carpathians (Poland)
Previous Article in Journal
No Evidence for Wolbachia Effects on the Thermal Preference of the Invasive Pest Liriomyza huidobrensis
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Prevalence of Borrelia and Rickettsia in Ixodes ricinus from Chosen Urban and Protected Areas in Poland and the Czech Republic

1
Department of Microbial Ecology and Acaroentomology, University of Wrocław, 51-148 Wrocław, Poland
2
Institute of Experimental Biology, Faculty of Science, Masaryk University, 60200 Brno, Czech Republic
3
Department of Biology, Faculty of Education, Masaryk University, 60200 Brno, Czech Republic
*
Author to whom correspondence should be addressed.
Insects 2024, 15(10), 785; https://doi.org/10.3390/insects15100785
Submission received: 16 September 2024 / Revised: 4 October 2024 / Accepted: 4 October 2024 / Published: 9 October 2024
(This article belongs to the Special Issue Women’s Special Issue Series: Insects)

Abstract

:

Simple Summary

Ixodes ricinus, the most important tick vector in Europe, is responsible for the spreading of medically important pathogens. This study aimed to detect Borrelia spp. and Rickettsia spp. in I. ricinus ticks collected in urban and protected areas both in Poland and the Czech Republic. Ixodes ricinus ticks collected in Poland compared to ticks from the Czech Republic were more infected with Borrelia spp., and ticks collected in protected areas were more infected with Borrelia spp. than ticks collected in urban areas. Rickettsia spp. prevalence in I. ricinus was comparable in both Poland and the Czech Republic; however, regional differences were observed. The regional differences in Borrelia spp. and Rickettsia spp. prevalence in I. ricinus indicate the need for adaptation of public health surveillance strategies in each region.

Abstract

(1) Background: Ixodes ricinus is responsible for the spreading of medically important pathogens. Monitoring the level of tick infection in various areas is essential for determining the potential tick-born risk. This study aimed to detect Borrelia spp. and Rickettsia spp. in I. ricinus ticks collected in urban and protected areas both in Poland and the Czech Republic. (2) Methods: Ticks were collected by flagging in the years 2016–2017. Borrelia spp. was detected using nested PCR targeting the flaB gene and Rickettsia spp. using nested PCR targeting gltA. (3) Results: In total, DNA of Borrelia spp. was detected in 25.9% of samples. Ticks collected in Poland were more infected compared to the Czech Republic and ticks collected in protected areas were more infected with Borrelia spp. than ticks collected in urban areas. The RFLP analysis showed the occurrence of B. afzelii and B. garinii in both countries, and additionally B. valaisiana, B. burgdorferi s.s., and B. miyamotoi in Poland. Rickettsia spp. was detected in 17.4% of I. ricinus, with comparable infection level in both countries; however, regional differences were observed. (4) Conclusion: The regional differences in Borrelia spp. and Rickettsia spp. prevalence in I. ricinus indicate the complexity of factors influencing the level of infection and underline the need for adaptation public health surveillance strategies in each region.

1. Introduction

Ixodes ricinus, one of the best-known tick vectors in the world, is responsible for the spreading of tick-borne diseases in Europe, including Poland and the Czech Republic. Both in Poland and the Czech Republic, I. ricinus exists throughout the country [1,2,3] and is responsible for transmitting majority of tick-borne pathogens of medical importance, including Lyme borreliosis (LB). Lyme borreliosis remains still the most-often detected tick-borne diseases in Europe with the highest seroprevalence in countries in Western and Eastern Europe [4,5,6]. However, estimates of LB incidence vary not only in neighbouring countries, but also at the subnational level [5]. In Poland, over the last decade 2014–2023, according to the National Institute of Public Health NIH—National Research Institute [7], the incidence of LB ranged from 32.8 cases per 100,000 population in 2021 to 66.92 in 2023. In the Czech Republic, over the last decade 2014–2023, based on the data published by the National Institute of Public Health [8], cases of LB ranged from 25.7 cases per 100,000 population in 2021 to 42.9 cases in 2018. However, it is necessary to accept the idea that not all cases of the disease were reported to the system, so the actual number of cases may be higher. Furthermore, both in Poland and the Czech Republic, the variations in the number of notified cases are observed within the country. In Poland in 2022, when over 45.9/100,000 cases were recorded, the incidence ranged from 22.6 in Łódź voivodeship to 81.2 in Podlaskie voivodeship. In the Czech Republic, for example, in May 2023, during the spring period when high activity of ticks can be expected, 41 patients with LB were notified in the South Bohemian Region and only 3 patients in the capital city of Prague. The South Bohemian region is a rural part of the country where the population is approximately two-thirds that of Prague.
In addition to Borrelia spp., responsible for LB (B. burgdorferi s.l. group), I. ricinus can transmit Borrelia, responsible for relapsing fever (B. miyamotoi group), which are more recently described in human pathology [9]. Borrelia miyamotoi, first isolated from I. persulcatus ticks in Japan in the 1990s, is now known almost throughout the northern hemisphere, including Asia, Europe, and America. Infections caused by B. miyamotoi (Borrelia miyamotoi disease, BMD) are much less frequently diagnosed compared to B. burgdorferi s.l. [10]. The first case of B. miyamotoi spirochete infection in a human was noted in 2011 in Russia. Since then, B. miyamotoi infections have been diagnosed in North America, Asia (China, Japan), and Europe. In Poland, the first detection of B. miyamotoi DNA in a patient was described in 2019 [11].
Ixodes ricinus is also known to transmit tick-borne rickettsioses, including Rickettsia helvetica, which is frequently noted throughout Europe [12]. This Rickettsia, first isolated in 1979 from I. ricinus in Switzerland, was described in 1993 as a distinct species of the spotted fever group of rickettsiae named R. helvetica [13]. It seems that the pathogenicity of R. helvetica varies between patients, from asymptomatic infection with non-specific clinical signs with mild and self-limiting courses to serious symptoms [9,12,14,15]. In Poland, according to the National Institute of Public Health NIH—National Research Institute [7], a few human cases of spotted fever and other rickettsioses are noticed per year; however, it is not distinguished whether they are caused by R. helvetica or another Rickettsia species. In the Czech Republic, rickettsioses and the occurrence of antibodies against Rickettsia spp. are not routinely investigated. Although it has been confirmed that ticks in the Czech Republic contain Rickettsia spp., only rare cases of human infections were reported. On the website of the State Health Institute [8], the number of confirmed cases of rickettsiosis can be found, showing that in past 10 years, a total of 58 cases have been reported. However, it is not possible to trace a specific type of disease caused by a certain type of pathogenic rickettsia. Moreover, rickettsioses do not show any characteristic symptoms such as fever and rash, but even then they can easily be confused with other diseases with similar symptoms. Rickettsia slovaca, transmitted mainly by ticks of the Dermacentor genus and R. monacensis and R. helvetica, which are transmitted by the I. ricinus, are considered to be the main candidates for spreading this type of infection in the Czech Republic [8].
The increase in outdoor activities among Europeans extends contact with ticks and consequently increases the risk of tick-borne diseases [16]. A rise in the incidence of LB over the last decades and the detection of new tick-borne pathogens indicates the need for systematic monitoring the potential health tick-borne risks. In Central Europe, I. ricinus inhabits mainly broad-leaved and mixed forests and forest-like habitats, but the tick can also be found in suburban locations [17]. Moreover, infected I. ricinus may be present both in forest and urban green spaces, including urban parks and gardens with suitable microclimate and host availability [18]. Therefore, determining the level of tick infection in various areas, including diversity in geographical location and the impact of anthropopressure, is crucial for determining potential tick-born risk. This study aimed to assess the infection level with Borrelia and Rickettsia among I. ricinus ticks collected in chosen urban and protected areas both in Poland and the Czech Republic.

2. Materials and Methods

2.1. Tick Sampling

Ticks were collected by flagging vegetation in the years 2016–2017 in four localities (Figure 1), including urban and protected areas both in south-western Poland and south-eastern Czech Republic. Urban areas covered city parks in communal forests in the conurbation of Wrocław (Poland) and Brno (the Czech Republic), while protected areas were located in forests of the Ślęża Landscape Park (Poland), and the Moravian Karst Protected Landscape Area (the Czech Republic). Wrocław (51°6′ N 17°2′ E), the capital of the Lower Silesia region located on the banks of the Odra River, 105–156 m above sea level, is the fourth largest city in Poland with a population of ca 640,000 inhabitants. The town is characterised by a temperate transitional climate subject to continental and oceanic influences, with the annual average temperature estimated at ca 10 °C and a mean annual precipitation of 567 mm [19]. The urban green spaces cover 34.0% of the city area and a total area of parks and communal forests in Wroclaw account for ca 530 ha [19]. The Ślęża Landscape Park (ŚLP), established in 1988, with the highest elevation ofŚlęża (717 m a.s.l.), is located about 40 km southwest of Wrocław and covers an area of ca 7600 ha [20]. The ŚLP is very popular among tourists and cyclists because the natural habitats in ŚLP include forest, rocky, meadow, and grassland habitats threatened due to anthropogenic impacts [21]. To protect the most valuable floristic, landscape, and historical areas, three nature reserves were created within ŚPK. In Brno (49°12′ N 16°37′ E), the conurbation of the locality of Pisarky was chosen. Pisarky, located 2 km far from the centre of the town, is situated 197–210 m above sea level and forms the bottom of Pisarky vale. On the hillside of this valley, a mixed wood as a park wood for the people’s holiday utilisation is growing. In this biotype, the predominant trees are Quercus petraea, Q. robur, Carpinus betulus, and Pinus silvestris. The annual average temperature is ca 8.9 °C and the mean annual precipitation is 559 mm. The environment of the Moravian Karst Protected Landscape Area (MKPLA, 49°21′ N, 16°42′ E) is situated in the surrounding of Skalní mlýn, with preserved species in beech forests. In the upper warmer parts, there are oak and horn beam forests with rivers and extremely wet meadows. The site extends around the emergence of the river Punkva, the best-developed karst phenomena. The annual average temperature is estimated at ca. 7.7 °C and a mean annual precipitation of 600 mm, situated 334 m above sea level. The collected ticks were identified at the species level with the use of a key for Ixodida identification [22].

Borrelia spp. and Rickettsia spp. Detection

The molecular study covered 413 individual Ixodes ricinus ticks, including 235 ticks (190 nymphs, 27 females, 18 males) collected in Poland (91 in Wrocław and 144 in ŚLP), and 178 ticks (119 nymphs, 30 females, 29 males) from the Czech Republic (72 from Brno and 106 from MKPLA). Both nymphs and adults were tested individually, and DNA extraction was carried out with the ammonium hydroxide (NH4OH) method by Stańczak et al. [23]. For the detection of Borrelia spp., the specific nested PCR targeting flaB gene-encoding flagellin [24], and for the detection of Rickettsia spp., primers targeting gltA gene-encoding citrate synthase were used [25,26]. Both nested PCR reactions were carried out with the use of PCR Mix Plus (A&A Biotechnology, Warszawa, Poland) and Thermal Cycler T100 (BioRad T100™ Thermal Cycler, Warszawa, Poland). The PCR mixture for Borrelia (25 μL total volume) consisted of 12.5 μL 2 × PCR Mix Plus (A&A Biotechnology), 2.5 μL of each primer, 4.5 μL sterile nuclease-free water, and 3 μL of template DNA for the first reaction, and 12.5 μL-2 × PCR Mix Plus (A&A Biotechnology), 2.5 μL of each primer, 5.5 μL sterile nuclease-free water, and 2 μL of the outer PCR product for nested PCR. The flaB gene for Borrelia spp. was amplified using the following thermal cycling programme: 95 °C for 3 min, 35 cycles at 95 °C for 45 s, 50 °C (132f i 905r) or 54 °C (220f i 824r) for 45 s, 72 °C for 1 min, followed by a final extension at 72 °C for 5 min. The reaction mixture for a single sample for Rickettsia spp. had a volume of 25 μL: 12.5 μL 2 × PCR Mix Plus (A&A Biotechnology), 1.25 μL of each primer, 5 μL sterile nuclease-free water, and 5 μL of template DNA for the first reaction, and 12.5 μL-2 × PCR Mix Plus (A&A Biotechnology), 1.25 μL of each primer, 8 μL-sterile nuclease-free water, and 2 μL of the outer PCR product for nested PCR. PCR reactions for Rickettsia spp. were as follows: 95 °C for 2 min, 35 cycles at 95 °C for 30 s, 50 °C (877p and 1258n) or 48 °C (896p and 1233n) for 30 s, and 72 °C for 1 min at the final elongation step at 72 °C for 5 min.
The PCR products were separated on 1.5% agarose gel (30 min, 100 V), and results were observed under a UV light transluminator. For identifying the genospecies of Borrelia spp., the RFLP method was used. The nested PCR positive samples were treated with the restriction enzyme HpyF3I (FastDigest HpyF3I, ThermoScientific, Waltham, MA, USA) according to Wodecka [27]. Restriction patterns obtained after electrophoresis in 3% agarose gel (75 min, 65 V) were observed under UV light and assigned to appropriate genospecies.

2.2. Statistic

To assess the relationship between pathogen infection levels and tick developmental stages (nymphs, females, and males), as well as between pathogen infection levels and study areas, a Chi-square test with p < 0.05 was used. Statistical analyses were performed using Statistica software version 12.0.

3. Results

In total, the DNA of Borrelia spp. was detected in 25.9% (107/413) of ticks (Table 1), with males being more infected (44.7%) compared to nymphs (23.3%) and females (24.5%) (χ2 = 9.777, p = 0.0075). Infected ticks were found both in the Czech Republic and Poland; however, I. ricinus collected in Poland were more infected compared to the Czech Republic (36.2% and 12.9%, respectively; χ2 = 28.348, p < 0.001). Ixodes ricinus collected in protected areas both in Poland and the Czech Republic were more infected, with Borrelia spp. than ticks collected in urban areas (48.6% vs. 16.5% in Poland, and 18.9% vs. 4.2% in the Czech Republic; χ2 = 24.93, p < 0.001; χ2 = 8.236, p = 0.0041, respectively).
The RFLP analysis of 57 samples positive in nested PCR proved five restriction patterns: four from the B. burgdorferi s.l. complex (B. afzelii, B. garinii, B. valaisiana, and B. burgdorferi s.s.) and one B. miyamotoi (Table 2). The dominant species of Borrelia spp. was B. garinii (42%), followed by B. afzelii (35%). Borrelia valaisiana (9%) and B. burgdorferi s.s. (3.5%) were found less frequently. Borrelia afzelii and B. garinii were detected both in Poland and the Czech Republic, whereas B. valaisiana and B. burgdorferi s.s. were only detected in Poland. Borrelia miyamotoi was identified in 10.5% Borrelia samples. Moreover, B. miyamotoi was found only in Poland, both in urbanised and protected areas.
Rickettsia spp. was detected in 17.4% (72/413) of I. ricinus (Table 1). Females were more infected compared to nymphs and males (33.3% vs. 14.6% and 17.0%; χ2 = 12.032, p = 0.002). The overall level of infection recorded in Poland and the Czech Republic was comparable, and the share was 18.7% and 15.7%, respectively (χ2 = 0.006, p = 0.9383). However, in the Czech Republic, more infected ticks were found in MKLPA than in Brno (21.7% vs. 6.9%; χ2 = 7.041, p = 0.008) and in Poland more in Wrocław than in ŚLP (26.4% vs. 13.9%; χ2 = 5.711, p = 0.0169).
Of the total 413 ticks, 13 ticks (3.0%), including 3 from MKLPA, 5 from ŚPK, and 5 from Wrocław, were co-infected with Borrelia spp. and Rickettsia spp. (Table 3). Co-infections were most often found in females and were less frequently found in males and nymphs (χ2 = 7.577, p = 0.0226). Additionally, in Wrocław, also, one co-infection of B. garinii and B. miyamotoi was noted.

4. Discussion

In the present study, the DNA of Borrelia was detected in Ixodes ricinus collected both in the Czech Republic and Poland; however, one of the most striking observations from our study is the significantly higher prevalence of Borrelia spp. among tick populations in Poland compared to the Czech Republic (36.2% vs. 12.9%). A potentially higher level of tick infection with Borrelia in Poland than in the Czech Republic has also been shown in other studies. The extensive literature review on B. burgdorferi s.l.’s prevalence in I. ricinus in peri/urban areas across Europe during the period 1990–2021 showed that adults and nymphs collected in Poland seem to be more infected than collected in the Czech Republic [18]. This finding suggests a notable difference in the risk of Lyme borreliosis (LB) transmission between the two countries. Several factors may contribute to this discrepancy, including the composition of tick microbiome and interactions within it, the viability of observed pathogens and their sensitivity to different factors, the variations in habitat characteristics, climatic conditions, the abundance and diversity of host species populations, the abundance and activity of ticks and vector species in general, landscape management, and many other factors which can influence pathogen transmission dynamics [28,29,30]. The difference in Borrelia spp.’s prevalence in Poland compared to the Czech Republic observed in our study underscores the need for tailored public health interventions and surveillance strategies in each region. In Poland, where Borrelia prevalence is notably higher, targeted efforts to raise awareness about LB risk and promote preventive measures such as tick avoidance and prompt tick removal are imperative. The need to raise awareness of tick-borne diseases was also found in surveys carried out among Czech and Polish university students of science [31]. The results obtained from the questionnaires show that the students of both countries were aware of the tick-born risks; however, they had only a superficial knowledge concerning tick-borne infections. Furthermore, the Czechs felt more at risk by ticks, and compared to the Poles, recognised the repellents as more effective.
In both countries, I. ricinus ticks collected in protected areas were more infected with Borrelia than ticks collected in urban areas. A similar pattern was noted in Slovakia, where the lowest prevalence was detected in the urban/suburban habitat than in the natural and agricultural habitat [32]. However, the result is not consistent with the meta-analysis of B. burgdorferi s.l.’s prevalence in questing I. ricinus in Europe, which shows that prevalence in peri/urban green space appears to be slightly higher compared to the average prevalence in Europe, which includes both urban and rural locations [18]. Nevertheless, this finding suggests that urbanisation through changes in host composition and modifications of habitat are likely to have an impact on Borrelia infection levels in ticks. However, a thorough understanding of the impact of urbanisation should be further investigated. Additionally, enhanced surveillance of tick populations in a diverse range of environments, understanding the effects of local habitat, and thorough analyses of LB human cases can help identify high-risk areas and guide targeted interventions.
In Europe, the species from the B. burgdorferi s.l. group most often causing LB in humans include B. burgdorferi s.s., B. garinii, B. afzelii, and, less frequently, B. spielmanii and B. bavariensis [9]. In our study, we found that, in both countries, B. garinii and B. afzelii were the most often detected genospecies. It is in line with a previous study conducted in Europe, where the meta-analysis of reports published between 2010 and 2016 shows that B. afzelii and B. garinii were the most frequently detected genospecies [33]. The presence of both B. afzelii and B. garinii indicates a diverse animal reservoir because B. afzelii is usually linked to rodents and B. garinii to birds [9]. Additionally, in Poland, in the B. burgdorferi s.l. complex, B. valaisiana and B. burgdorferi s.s. were determined, but they occurred less frequently. The knowledge of the distribution of particular genospecies is particularly important for epidemiologists due to various clinical outcomes [34].
In our study, among the identified Borrelia species, in the Czech Republic only spirochetes from the Borrelia burgdorferi s.l. group were found, while in Poland, in addition to B. burgdorferi s.l., B. miyamotoi was also noted. Perhaps the lack of B. miyamotoi presence in the Czech Republic is due to the relatively small number of ticks tested, because other studies show the presence of B. miyamotoi in the Czech Republic tick population. However, the estimated prevalence is low. Crowder et al. [35] detected B. miyamotoi in 8 ticks among 435 tested (1.8%), Honig et al. [36] in 2.1% (in 9 of the 435), and Bubanová et al. [37] in 2.0% (in 10 of the 505). In Poland, the presence of B. miyamotoi was confirmed in questing I. ricinus both in urban and wild areas; however, the prevalence was lower than in the case of LB spirochetes [38,39].
In contrast to Borrelia, our analysis reveals a comparable prevalence of Rickettsia spp. between Poland and the Czech Republic; however, differences in prevalence were observed at the subnational level. In the Czech Republic, more infected ticks were found in landscape parks than in urban areas (21.7% vs. 6.9%); in Poland, on the contrary, the infection was higher in urban areas than in landscape park (26.4% vs. 13.9%). The long-term study at Pisárky Park, i.e., locality covered also by current research, showed that from a total of 2813 I. ricinus ticks collected from 1996 to 2002, the mean positivity was 5.8% [40], which is similar to our results at the same place. A previous study conducted in the Czech Republic showed a higher minimal infection rate (3.4%) in a natural rather than an urban (2.9%) ecosystem [41], whereas in Poland, the prevalence of Rickettsia spp. was higher in urban (6.5%) than natural (4.4%) areas [42]. However, it is worth emphasising that information on the occurrence of Rickettsia species in ticks both in the Czech Republic and Poland is still fragmentary. The variability in Rickettsia spp.’s prevalence underscores the complex epidemiological dynamics of tick-borne pathogens and highlights the importance of continuous disease risk assessments and monitoring. The congruence in Rickettsia spp.’s prevalence suggests that certain ecological and environmental factors may exert a uniform influence on the transmission of this pathogen across borders. In both Poland and the Czech Republic, the prevalence of Rickettsia spp. determined in our study highlights the importance of vigilance linked with tick-borne pathogens beyond the causative agent of Lyme borreliosis. Exposure to tick-borne Rickettsia is also evidenced by serological tests of foresters, which are a group particularly exposed to tick bites [14]. Given the potential medical importance of rickettsial infections, proactive measures to reduce tick exposure and improve diagnostic capabilities are essential.
From a medical point of view, co-infections may be of particular importance due to its possible impact on severity of the disease in humans. In our studies, we found co-infection Rickettsia and Borrelia spp. in 3% of I. ricinus, with females being more frequently co-infected compared to nymphs and male ticks. Although we did not confirm interactions between Borrelia and Rickettsia infection due to the small sample size, such an association was shown in a meta-analysis conducted by Raulf et al. [43]. Therefore, the coexistence of different pathogens should be considered to be one of the factors influencing the level of prevalence.

5. Conclusions

Our study points out the regional differences in Borrelia spp. and Rickettsia spp. prevalence between Poland and the Czech Republic. By identifying these differences, we provide new insights for public health authorities and policymakers to develop targeted strategies for tick-borne disease prevention and control. However, further research is needed to clarify the underlying factors driving these discrepancies and to enhance our understanding of tick-borne pathogens issues in diverse ecological habitats.

Author Contributions

D.K.: conceptualization, methodology, investigation, formal analysis, data curation, writing the original draft; D.D.: methodology, formal analysis, data curation, investigation, writing the original draft; A.Ž.: investigation, writing the original draft; H.N.: investigation, writing the original draft. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. The research was financed by the University of Wrocław (research fundings).

Data Availability Statement

All data are contained within the manuscript.

Conflicts of Interest

The authors declare no competing interests.

References

  1. Dusbabek, F. Present state of research on ticks (Ixodoidea) in the Czech Republic. Wiad. Parazytol. 1995, 41, 267–276. [Google Scholar] [PubMed]
  2. Nowak-Chmura, M.; Siuda, K. Ticks of Poland. Review of contemporary issues and latest research. Ann. Parasitol. 2012, 58, 125–155. [Google Scholar]
  3. Otranto, D.; Dantas-Torres, F.; Santos-Sliva, M.M. Ixodes ricinus (Linnaeus, 1758) (Figs. 67–69). In Ticks of Europe and North Africa. A Guide to Species Identification; Estrada-Peña, A., Mihalca, A.D., Petney, T.N., Eds.; Springer: Cham, Switzerland, 2017; pp. 189–196. [Google Scholar]
  4. Marques, A.R.; Strle, F.; Wormser, G.P. Comparison of Lyme Disease in the United States and Europe. Emerg. Infect. Dis. 2021, 27, 2017–2024. [Google Scholar] [CrossRef]
  5. Burn, L.; Vyse, A.; Pilz, A.; Tran, T.M.P.; Fletcher, M.A.; Angulo, F.J.; Gessner, B.D.; Moïsi, J.C.; Stark, J.H. Incidence of Lyme Borreliosis in Europe: A systematic review (2005–2020). Vector Borne Zoonotic. Dis. 2023, 23, 172–194. [Google Scholar] [CrossRef]
  6. Stark, J.H.; Pilz, A.; Jodar, L.; Moïsi, J.C. The epidemiology of Lyme borreliosis in Europe: An updated review on a growing public health issue. Vector Borne Zoonotic. Dis. 2023, 23, 139–141. [Google Scholar] [CrossRef]
  7. National Institute of Public Health NIH—National Research Institute. Available online: https://wwwold.pzh.gov.pl/oldpage/epimeld/index_p.html (accessed on 30 May 2024).
  8. National Institute of Public Health. Available online: www.szu.cz (accessed on 30 May 2024).
  9. Boulanger, N.; Boyer, P.; Talagrand-Reboul, E.; Hansmann, Y. Ticks and tick-borne diseases. Med. Mal. Infect. 2019, 49, 87–97. [Google Scholar] [CrossRef]
  10. Sawczyn-Domańska, A. Occurrence and pathogenicity of Borrelia miyamotoi. Med. Og. Nauk. Zdr. 2021, 27, 343–348, (In Polish with English Abstract). [Google Scholar] [CrossRef]
  11. Fiecek, B.; Lewandowska, G.; Roguska, U.; Rozej-Bielicka, W.; Tylewska-Wierzbanowska, S.; Chmielewski, T. Borrelia miyamotoi DNA in a patient suspected of Lyme borreliosis. Res. Sq. 2019; preprint. [Google Scholar] [CrossRef]
  12. Azagi, T.; Hoornstra, D.; Kremer, K.; Hovius, J.W.R.; Sprong, H. Evaluation of disease causality of rare Ixodes ricinus-borne infections in Europe. Pathogens 2020, 9, 150. [Google Scholar] [CrossRef]
  13. Beati, L.; Péter, O.; Burgdorfer, W.; Aeschlimann, A.; Raoult, D. Confirmation that Rickettsia helvetica sp. nov. is a distinct species of the spotted fever group of rickettsiae. Int. J. Syst. Bacteriol. 1993, 43, 521–526. [Google Scholar] [CrossRef]
  14. Borawski, K.; Dunaj, J.; Czupryna, P.; Pancewicz, S.; Świerzbińska, R.; Żebrowska, A.; Moniuszko-Malinowska, A. Prevalence of spotted fever group Rickettsia in North-Eastern Poland. Infect. Dis. 2019, 51, 810–814. [Google Scholar] [CrossRef]
  15. Borawski, K.; Dunaj, J.; Pancewicz, S.; Król, M.; Czupryna, P.; Moniuszko-Malinowska, A. Tick-borne rickettsioses in Europe—A review. Przegl. Epidemiol. 2019, 3, 523–530. [Google Scholar] [CrossRef] [PubMed]
  16. Parola, P.; Raoult, D. Tick-borne bacterial diseases emerging in Europe. Clin. Microbiol. Infect. 2021, 7, 80–83. [Google Scholar] [CrossRef]
  17. Kahl, O.; Gray, J.S. The biology of Ixodes ricinus with emphasis on its ecology. Ticks Tick-Borne Dis. 2023, 14, 102114. [Google Scholar] [CrossRef]
  18. Hansford, K.M.; Wheeler, B.W.; Tschirren, B.; Medlock, J.M. Questing Ixodes ricinus ticks and Borrelia spp. in urban green space across Europe: A review. Zoonoses Public Health 2022, 69, 153–166. [Google Scholar] [CrossRef]
  19. Blachowski, J.; Hajnrych, M. Assessing the cooling effect of four urban parks of different sizes in a temperate continental climate zone: Wroclaw (Poland). Forests 2021, 12, 1136. [Google Scholar] [CrossRef]
  20. Krajewski, P.; Solecka, I.; Mrozik, K. Forest landscape change and preliminary study on its driving forces in Ślęża Landscape Park (Southwestern Poland) in 1883–2013. Sustainability 2018, 10, 4526. [Google Scholar] [CrossRef]
  21. Świerkosz, K. Natural habitats of the Ślężański Landscape Park—State of protection and threats. In Proceedings of the Konferencja Naukowa z okazji 25-Lecia Ślężańskiego Parku Krajobrazowego. Istniejące i Potencjalne Zagrożenia Funkcjonowania Parków Krajobrazowych, Sobótka, Poland, 10–11 October 2013; Śniegucki, P., Krajewski, P., Eds.; Dolnośląski Zespół Parków Krajobrazowych: Wroclaw, Poland, 2013; pp. 73–81, (In Polish with English Abstract). [Google Scholar]
  22. Estrada-Peña, A.; Michalca, A.D.; Peteney, T.N. Ticks of Europe and North Africa. A Guide to Specimen Identification; Springer: Cham, Switzerland, 2017; ISBN 978-3-319-63759-4. [Google Scholar] [CrossRef]
  23. Stańczak, J.; Racewicz, M.; Kubica-Biernat, B.; Kruminis-Lozowska, W.; Dabrowski, J.; Adamczyk, A.; Markowska, M. Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks (Acari, Ixodidae) in different Polish woodlands. Ann. Agric. Environ. Med. 1999, 6, 127–132. [Google Scholar]
  24. Wodecka, B.; Rymaszewska, A.; Sawczuk, M.; Skotarczak, B. Detectability of tick-borne agents DNA in the blood of dogs, undergoing treatment for borreliosis. Ann. Agric. Environ. Med. 2009, 16, 9–14. [Google Scholar]
  25. Prakash, J.; Sohan, L.T.; Rosemol, V.; Verghese, V.; Pulimood, S.; Reller, M.; Dumler, J. Molecular detection and analysis of spotted fever group Rickettsia in patients with fever and rash at a tertiary care centre in Tamil Nadu, India. Pathog. Glob. Health 2012, 106, 40–45. [Google Scholar] [CrossRef]
  26. Miková, K.; Berthová, L.; Kalúz, S.; Kazimírová, M.; Burdová, L.; Kocianová, E. First detections of Rickettsia helvetica and R. monacensis in ectoparasitic mites (Laelapidae and Trombiculidae) infesting rodents in south-western Slovakia. Parasitol. Res. 2015, 114, 2465–2472. [Google Scholar] [CrossRef]
  27. Wodecka, B. FlaB Gene as a molecular marker for distinct identification of Borrelia species in environmental samples by the PCR-Restriction Fragment Length Polymorphism method. Appl. Environ. Microbiol. 2011, 77, 7088–7092. [Google Scholar] [CrossRef]
  28. Rizzoli, A.; Hauffe, H.; Carpi, G.; Vourc, H.G.; Neteler, M.; Rosa, R. Lyme borreliosis in Europe. Euro. Surveill. 2011, 16, 19906. [Google Scholar] [CrossRef]
  29. Roche, B.; Rohani, P.; Dobson, A.P.; Guégan, J.F. The impact of community organization on vector-borne pathogens. Am. Nat. 2013, 181, 1–11. [Google Scholar] [CrossRef] [PubMed]
  30. Bariod, L.; Saïd, S.; Calenge, C.; Chabot, S.; Badeau, V.; Bourgoin, G. Parasitized or non-parasitized, why? A study of factors influencing tick burden in roe deer neonates. PLoS ONE 2022, 17, e0262973. [Google Scholar] [CrossRef]
  31. Nejezchlebova, H.; Kiewra, D.; Žákovská, A.; Ovesná, P. Students’ attitudes to tick risks. Ann. Agric. Environ. Med. 2016, 23, 437–441. [Google Scholar] [CrossRef]
  32. Kazimírová, M.; Mahríková, L.; Hamšíková, Z.; Stanko, M.; Golovchenko, M.; Rudenko, N. Spatial and temporal variability in prevalence rates of members of the Borrelia burgdorferi species complex in Ixodes ricinus ticks in urban, agricultural and sylvatic habitats in Slovakia. Microorganisms 2023, 11, 1666. [Google Scholar] [CrossRef]
  33. Strnad, M.; Hönig, V.; Růžek, D.; Grubhoffer, L.; Rego, R.O.M. Europe-Wide Meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Appl. Environ. Microbiol. 2017, 83, e00609-17. [Google Scholar] [CrossRef] [PubMed]
  34. Estrada-Peña, A.; Cutler, S.; Potkonjak, A.; Vassier-Tussaut, M.; Van Bortel, W.; Zeller, H.; Fernández-Ruiz, N.; Mihalca, A.D. An updated meta-analysis of the distribution and prevalence of Borrelia burgdorferi s.l. in ticks in Europe. Int. J. Health Geogr. 2018, 17, 41. [Google Scholar] [CrossRef]
  35. Crowder, C.D.; Carolan, H.E.; Rounds, M.A.; Honig, V.; Mothes, B.; Haag, H.; Nolte, O.; Luft, B.J.; Grubhoffer, L.; Ecker, D.J.; et al. Prevalence of Borrelia miyamotoi in Ixodes ticks in Europe and the United States. Emerg. Infect. Dis. 2014, 20, 1678–1682. [Google Scholar] [CrossRef]
  36. Honig, V.; Carolan, H.E.; Vavruskova, Z.; Massire, C.; Mosel, M.R.; Crowder, C.D.; Rounds, M.A.; Ecker, D.J.; Ruzek, D.; Grubhoffer, L.; et al. Broad-range survey of vector-borne pathogens and tick host identification of Ixodes ricinus from Southern Czech Republic. FEMS Microbiol. Ecol. 2017, 93, 129. [Google Scholar] [CrossRef] [PubMed]
  37. Bubanová, D.; Fučíková, A.M.; Majláth, I.; Pajer, P.; Bjelková, K.; Majláthová, V. The first detection of relapsing fever spirochete Borrelia miyamotoi in Ixodes ricinus ticks from the northeast Czech Republic. Ticks Tick. Borne Dis. 2022, 13, 102042. [Google Scholar] [CrossRef] [PubMed]
  38. Kiewra, D.; Stańczak, J.; Richter, M. Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in Lower Silesia, Poland-preliminary study. Ticks Tick. Borne Dis. 2014, 5, 892–897. [Google Scholar] [CrossRef]
  39. Kowalec, M.; Szewczyk, T.; Welc-Falęciak, R.; Siński, E.; Karbowiak, G.; Bajer, A. Ticks and the city—Are there any differences between city parks and natural forests in terms of tick abundance and prevalence of spirochaetes? Parasit. Vectors 2017, 10, 573. [Google Scholar] [CrossRef]
  40. Zákovská, A.; Vostal, K.; Martiníková, H. A longitudinal study of the prevalence of borreliae in ticks in the urban locality of Brno-Pisárky, Czech Republic. J. Vector. Ecol. 2008, 33, 385–388. [Google Scholar] [CrossRef]
  41. Venclikova, K.; Rudolf, I.; Mendel, J.; Betasova, L.; Hubalek, Z. Rickettsiae in questing Ixodes ricinus ticks in the Czech Republic. Ticks Tick-Borne Dis. 2014, 5, 135–138. [Google Scholar] [CrossRef]
  42. Kowalec, M.; Szewczyk, T.; Welc-Falęciak, R.; Siński, E.; Karbowiak, G.; Bajer, A. Rickettsiales occurrence and co-occurrence in Ixodes ricinus ticks in natural and urban areas. Microb. Ecol. 2019, 77, 890–904. [Google Scholar] [CrossRef]
  43. Raulf, M.K.; Jordan, D.; Fingerle, V.; Strube, C. Association of Borrelia and Rickettsia spp. and bacterial loads in Ixodes ricinus ticks. Ticks Tick-Borne Dis. 2018, 9, 18–24. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Tick monitoring sites in Poland and the Czech Republic.
Figure 1. Tick monitoring sites in Poland and the Czech Republic.
Insects 15 00785 g001
Table 1. Borrelia spp. and Rickettsia spp. detected in Ixodes ricinus ticks collected in urban and protected areas in Poland and the Czech Republic.
Table 1. Borrelia spp. and Rickettsia spp. detected in Ixodes ricinus ticks collected in urban and protected areas in Poland and the Czech Republic.
CountySiteIxodes ricinus Developmental Stage
Number of Infected/Number of Investigated
Borrelia spp.Rickettsia spp.
NymphFemaleMaleTotalNymphFemaleMaleTotal
Czech
Republic
Brno3/610/50/63/72
(4.2%)
3/611/51/65/72
(6.9%)
MKLPA12/580/258/2320/106
(18.9%)
7/5811/255/2323/106
(21.7%)
Total15/1190/308/2923/178
(12.9%)
10/11912/306/2928/178
(15.7%)
PolandWrocław11/694/170/515/91
(16.5%)
17/697/170/524/91
(26.45)
ŚLP47/12110/1013/1370/144
(48.6%)
18/1210/102/1320/144
(13.9%)
Total58/19014/2713/1885/235
(36.2%)
35/1907/272/1844/235
(18.7%)
Total72/309
(23.3%)
14/57
(24.5%)
21/47
(44.7%)
107/413
(25.9%)
45/309
(14.6%)
19/57
(33.3%)
8/47
(17.0%)
72/413
(17.4%)
Table 2. Borrelia genospecies detected in Ixodes ricinus ticks collected in Poland and the Czech Republic.
Table 2. Borrelia genospecies detected in Ixodes ricinus ticks collected in Poland and the Czech Republic.
CountyIxodes ricinusBorrelia burgdorferi s.l. (%)B. miyamotoi
(%)
B. afzeliiB. gariniiB. valaisianaB. burgdorferi s.s.
Czech Republic Nymph31---
Female -----
Male1----
Total41---
PolandNymph129315
Female21021-
Male24--1
Total1623526
Total20 (35%)24 (42%)5 (9%)2 (3.5%)6 (10.5%)
Table 3. Coinfection of Borrelia spp. and Rickettsia spp. in Ixodes ricinus ticks collected in Poland and the Czech Republic.
Table 3. Coinfection of Borrelia spp. and Rickettsia spp. in Ixodes ricinus ticks collected in Poland and the Czech Republic.
CountySiteIxodes ricinus Developmental Stage
Number of Coinfected/Number of Investigated
(%)
NymphFemaleMaleTotal
Czech RepublicBrno0/610/50/60/72
MKLPA1/582/250/233/106
PolandWrocław2/693/170/55/91
ŚLP3/1210/102/135/144
Total6/309 (1.9%)5/57 (8.8%)2/47(4.3%)13/413(3.0%)
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Kiewra, D.; Dyczko, D.; Žákovská, A.; Nejezchlebova, H. Prevalence of Borrelia and Rickettsia in Ixodes ricinus from Chosen Urban and Protected Areas in Poland and the Czech Republic. Insects 2024, 15, 785. https://doi.org/10.3390/insects15100785

AMA Style

Kiewra D, Dyczko D, Žákovská A, Nejezchlebova H. Prevalence of Borrelia and Rickettsia in Ixodes ricinus from Chosen Urban and Protected Areas in Poland and the Czech Republic. Insects. 2024; 15(10):785. https://doi.org/10.3390/insects15100785

Chicago/Turabian Style

Kiewra, Dorota, Dagmara Dyczko, Alena Žákovská, and Helena Nejezchlebova. 2024. "Prevalence of Borrelia and Rickettsia in Ixodes ricinus from Chosen Urban and Protected Areas in Poland and the Czech Republic" Insects 15, no. 10: 785. https://doi.org/10.3390/insects15100785

APA Style

Kiewra, D., Dyczko, D., Žákovská, A., & Nejezchlebova, H. (2024). Prevalence of Borrelia and Rickettsia in Ixodes ricinus from Chosen Urban and Protected Areas in Poland and the Czech Republic. Insects, 15(10), 785. https://doi.org/10.3390/insects15100785

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop