Tick-borne infections represent a One Health concern to human and animal health. Ticks ectoparasitize their hosts at each stage of their life cycle and may transmit severe bacterial, parasitic, and viral pathogens. These pathogens can induce behavioural changes in ticks and affect their phenotypic characteristics, making them more active in host-seeking and more resistant against extreme environmental events (e.g. desiccation and cold), which consequently leads to increased fitness and survival (22).
The transmission of pathogens from ticks to hosts depends mainly on the duration of host attachment. For instance, TBEV can be transmitted within only 15–60 min of attachment. However, other microorganisms require a longer period, ranging from 3 hours (such as Ehrlichia spp., Anaplasma spp., and Rickettsia spp.) to 2 days (Borrelia and protozoan parasites) (23). Transmission times may vary considerably between different tick vectors, pathogens, pathogen quantity, host species, and conditions; successful pathogen transmission may require feeding longer than 24–48 h in natural conditions, in contrast to intensive laboratory exposure (24, 25) .
Ticks require blood meals to develop to the next life stage. Consequently, infection rate may vary depending on developmental stage. In I. ricinus ticks in Denmark, the infection rate was 2.7 times higher in adults compared to nymphs. Coinfection rates were 12.3% in adult females and 3.5% in nymphs (26). In our study, 98.5% of the ticks from which data were available were adults. Only 1.5% were nymphs, as these are difficult to detect from pets. For the subset of ticks analysed, 53% of the ticks were engorged, which, together with the infection rate of 17.2% of these ticks, indicates that these pets were at risk of getting infection. This emphasizes the need for anti-tick medication for pets.
The estimates of tick abundance, microbial content, and infection rate of ticks may differ depending on the collection method (27). For instance, the commonly used cloth dragging method severely underestimates the abundance of ticks (28). In Spain, Del Cerro et al found mostly Borrelia spp. and Rickettsia slovaca in questing ticks only, while some pathogens, including “Candidatus Rickettsia rioja”, Rickettsia raoultii, and A. phagocytophilum were found in both questing ticks and ticks feeding on animals (27). Additionally, protozoan pathogens were detected in engorged animal-fed ticks except for Babesia bigemina, which was found only in questing ticks collected by dragging (27). Likewise, in Germany, Babesia spp. and A. phagocytophilum were most prevalent in engorged ticks collected from roe deer, followed by nymphs and adult questing ticks (29).
Our findings agree with previous studies in Finland, which reported I. ricinus and I. persulcatus as the prevalent tick species with medical/veterinary importance and their geographical distribution (3, 4, 30). These two tick species hybridize naturally, as shown by molecular genetic studies (31). Here, we found one hybrid tick that did not show a positive result for the studied pathogens. We also found one R. sanguineus that was positive for B. venatorum. It is noteworthy that the dog from which the tick was collected had a travel history with his owner in Spain, explaining its presence in Finland. The risk of importing exotic tick species and pathogens can be increased via traveling with animals without ectoparasitic treatment (6, 32).
Climate and environment play significant roles in the distribution of ticks and tick-borne diseases, as arthropods are especially sensitive to changes in climatic and environmental conditions. Based on the latest climate projections for Finland, mean air temperature is predicted to increase by 2.4°C in summer and by 3.3°C in winter by 2070 (33). Similarly, precipitation is estimated to increase by 5% during summer and by 12% during winter (33). Warmer temperature and higher precipitation during summer and winter in Finland are expected to impact ticks in several ways. Higher tick abundance, longer activity seasons, and range expansions of both native and invasive tick species are expected to occur. For example, the invasive tick species Hyalomma marginatum in migratory birds has already been occasionally reported in Finland (5). In the other northern European countries, the vector of Babesia canis, Dermacentor reticulatus, has been observed in dogs and migratory birds (34).
We encountered difficulties in tick species identification. The duplex qPCR that we used (13) was suitable to identify I. ricinus and I. persulcatus but not R. sanguineus. Therefore, we performed ITS2 PCR-based sequencing for all ticks. However, we were able to sequence only 79.5% (272) of the ticks. The reason for failure with the remaining 70 ticks may be due to the quality of the extracted DNA. For all sequenced DNAs, no incongruence was found between qPCR and ITS2 PCR-based sequencing. For R. sanguineus, both methods (ITS2 and Cox1 PCR-based sequencing) confirmed its identification. Misidentification of tick species is common. The misidentification rate of ticks collected in different countries and assessed by qualified experts has reached 29.6% (35).
Although information on the prevalence of tick-borne infections in companion animals is limited, infections caused by Borrelia, Anaplasma, Babesia, and TBEV have been reported in Northern European countries (1). In humans, LB and TBE are the most commonly registered tick-borne diseases in the Nordic countries, including Finland. According to national health care registers, the incidence of microbiologically and clinically confirmed human LB cases is increasing (36). Our results showed a prevalence of 10.5% for B. burgdorferi s.l. in ticks collected from pets 2020–2021, which is lower than the average prevalence in questing adult ticks of 48.9 ± 8.4% (37). In Finnish dogs, the seroprevalence of B. burgdorferi is low (2.9%) (8), and no antibodies to B. burgdorferi were detected in cats. Likewise, another seroprevalence study conducted elsewhere in Europe indicated the rarity of B. burgdorferi antibodies in feline samples (38). Dogs can become infected with B. burgdorferi and develop antibodies, but unlike humans, they rarely get sick. The signs in dogs include fever, fatigue, loss of appetite, intermittent lameness, and swollen and painful joints; skin rash is not observed in animals (39).
In contrast to B. burgdorferi s.l., B. miyamotoi showed a prevalence (1.5%, 95% confidence interval [CI] 0.5–3.4) that is similar to that reported in questing ticks from nationwide studies (0.7%) and in our recent larger collection of ticks from the capital region of Finland (0.6%) (37, 40). Our previous results also confirmed the circulation of B. miyamotoi in ticks from Finland without the detection of bacterial DNA in a large collection of human samples (40). However, clinical human infections caused by B. miyamotoi have been reported elsewhere, confirming its association with human, but not pet animal, disease (41).
We found TBEV in only one tick, representing a low prevalence and corresponding with another local study (37). The most recent nationwide study on a very large collection of ticks did not detect TBEV in ticks from Finland (37), although the previous nationwide study based on crowdsourcing conducted in 2015 showed a prevalence of 0.2% and 3.0% in I. ricinus and I. persulcatus, respectively (37). Overall, TBEV has a very focal distribution in ticks and extrapolating over larger areas is uncertain. In dogs, TBEV can cause severe and even fatal neurological symptoms, but the high seroprevalence in healthy dogs in some areas, such as in the Åland Islands, indicates that TBEV results mostly in subclinical infection (9). Further, dogs can be used as sentinels for TBEV and provide an idea for public health surveillance (42).
We detected A. phagocytophilum DNA in 12 ticks (3.5%, 95% CI 1.8–6.1), of which 3 infested a single animal. This prevalence is slightly higher than the prevalence reported in questing ticks (0.6%) (3). The seroprevalence of A. phagocytophilum in Finnish dogs is as high as 5.3%, indicating that infections are common in dogs (8).
Ehrlichia canis can cause a serious disease in dogs and is mainly transmitted by R. sanguineus, which is not endemic in Finland. In this study, the single R. sanguineus tick was imported from Spain and E. canis was not found. We did not detect E. canis in other ticks either. Its absence corresponds with the low seroprevalence of E. canis (0.3%) in dogs from Finland (8). Further, the presence of E. canis in the most common tick species from the Nordic countries (Ixodes sp.) has not been confirmed. However, a low prevalence was documented in I. ricinus ticks from the Netherlands (43).
Babesia spp. have medical and veterinary importance. According to the Finnish Food Authority, bovine babesiosis was last reported in 2021 (44). In Finnish humans, a fatal case due to B. divergens was reported in a previously ill man who was infected simultaneously with Borrelia in 2004 (45). We are unaware of any other cases at the time of this study. In the current study, B. venatorum was found in ticks (3 in I. ricinus and 1 in R. sanguineus) collected from Taivassalo, Jyväskylä, and Tampere, which are on the southern coast and central part of Finland. B. venatorum was detected in Finnish ticks collected in 2015 (30), although no human or animal cases have been reported in the country. However, animal and human infections due to B. venatorum have been reported elsewhere (46, 47).
The vector of Babesia canis, Dermacentor reticulatus, has not been reported in Finland. However, canine blood samples have confirmed the presence of B. canis DNA and reports have confirmed canine babesiosis in imported dogs (48, 49). Further, other Nordic countries have confirmed the occasional presence of D. reticulatus ticks on dogs, migratory birds, and in nature (34).
In addition to well-known tick-borne pathogens, we studied the prevalence of Ca. N. mikurensis, a bacterium emerging in Europe (50). This bacterium was recently detected in both I. ricinus and I. persulcatus in Finland (30). We found a prevalence of 0.9%, which is similar to that reported in I. ricinus (0.8%) (3). Ca. N. mikurensis causes disease in immunocompromised humans and has also been detected in a splenectomized dog (50, 51).
The availability of next-generation technologies means that high-throughput sequencing of the full 16S gene is becoming a reality for species and strain-level bacterial detection and could be used by veterinary laboratories for faster detection of a range of pathogens. In the future, full-length 16S rRNA gene sequencing of clinical samples may support species identification and provide important information on bacterial community differences between tick species and geographic locations. Optimally, follow-up samples would have been available from the animals to study transmission and survey the clinical relevance of the microbial findings. However, such samples were not available in this study and may be available in future studies.