Ticks Parasitizing Humans in Greece

Introduction

T icks are arthropods that belong to the class Arachnida and, along with other mites, constitute the order Acarina. They are blood-feeding parasites of mammals, birds, and reptiles. There are many species of ticks worldwide and categorized into three families: Argacidae (soft ticks) with 183 species, Ixodidae (hard ticks) with 683 species, and Nuttalliellidae (hard ticks) with 1 monospecific genus in Africa (Horak et al. 2002). The life cycle of ticks depends on climate, host populations, landscape characteristics, and the fine modulation of the populations of every partner involved; thus, a variety of geographical and climatic factors affect their distribution (Estrada-Pena 2009). Many ticks are considered as a threat to human and animal health, as they transmit pathogens through their saliva during feeding. Anthropophilic ticks are vectors of bacterial, viral, or parasitic diseases, like Lyme disease, rickettsiosis, anaplasmosis, ehrlichiosis, tick-borne encephalitis, Crimean-Congo hemorrhagic fever (CCHF), and babesiosis (Heyman et al. 2010).

Greece is a Balkan country with a Mediterranean climate, although various microclimates can be observed. The main tick genera found in Greece are Rhipicephalus, Ixodes, Hyalomma, Haemaphysalis, Dermacentor, Boophilus (which is now considered as subgenus of the genus Rhipicephalus), and Amblyomma (Papadopoulos et al. 1996, Pavlidou et al. 2008). Tick-borne diseases have been reported among humans in Greece, with most severe of them being CCHF, which emerged in the country in summer of 2008 (Papa et al. 2008, 2009). CCHF virus (CCHFV) is transmitted to humans by tick bite or by direct contact with viremic blood or tissues of patients or livestock. The geographic distribution of CCHFV is the most extensive of the tick-borne human viral pathogens, and coincides with the distribution of Hyalomma ticks. Hyalomma marginatum (Mediterranean Hyalomma) is considered the main vector of CCHFV in most parts of the Palaearctic region (Hoogstraal 1979). In addition, Mediterranean spotted fever (MSF) cases caused by Rickettsia conorii are often observed in Greece (Psaroulaki et al. 2006, Papa et al. 2008, 2010). MSF is transmitted by Rhipicephalus sanguineus (Rovery and Raoult 2008).

In June 2008 a woman, resident of Komotini city (Rodopi prefecture, Northeastern Greece), died after a tick bite; CCHF was laboratory confirmed (Papa et al. 2008). One month later, a man, resident of Aratos village (Rodopi prefecture, Northeastern Greece), presented similar symptoms and died; MSF was laboratory confirmed (Papa et al. 2010). Both patients had been hospitalized in Alexandroupolis University General Hospital. Immediately after the death of the CCHF patient, the Hellenic Center for Disease Control and Prevention developed public health interventions for the epidemiological investigation, and disseminated information regarding prevention of tick bites and proper removal of attached ticks to residents of and visitors to Rodopi prefecture; in addition, it informed the general population about CCHF and the preventive measures for tick bites (Maltezou et al. 2009). During summer 2008 an increased number of residents of Northeastern Greece referred to the hospitals in Komotini and Alexandroupolis for tick removal. The aims of the present study was to investigate the tick species that infested humans during this period and to have an insight into the potential of disease transmission through these parasites.

Materials and Methods

During June–September 2008, 537 ticks have been removed from humans by the medical staff of two hospitals of Northeastern Greece: Komotini General Hospital (300 ticks) and Alexandroupolis University General Hospital (237 ticks). Ticks collected from each person were stored in separate tubes containing 70% ethanol or formalin. Counting and identification of tick species, life stage, and sex were carried out under a dissecting stereomicroscope using identification keys, taking into account the external morphological characters (Estrada-Pena et al. 2004).

Results

Most ticks (519/537, 96.6%) were adults, and the rest (18/537, 3.4%) were larvae. All ticks belonged to three genera in the Ixodidae family: Rhipicephalus (469/519, 90.4%) with four species (R. sanguineus, R. turanicus, R. bursa, and R. [Boophilus] annulatus), Hyalomma (39/519, 7.51%) with three species (H. marginatum, H. rufipes, and H. anatolicum), and Ixodes (11/519, 2.12%) with two species (I. rinicus and I. gibbosus) (Table 1). The prevalence of R. sanguineus (81.5%) was significantly higher than that of the other species (p < 0.005), as it represented the 94.8% and 70.8% of the ticks in Alexandroupolis and Komotini, respectively. Female ticks were significantly more (485/519, 93.4%) than male (p < 0.005). Especially among R. sanguineus, 99.5% were females.

Most (61%) humans bitten by ticks were men. Age was available for 300 individuals of the study. No statistical difference was observed among groups (p > 0.5). However, the most affected age group was that of 0–9 years (20.3%), while the two following groups were those of 60–69 and 50–59 years (16.3% and 15%, respectively) (Table 2).

Discussion

A variety of diseases are transmitted to humans by ticks. An increased number of residents of Northeastern Greece visited hospitals and health care centers during summer 2008 for tick removal. This was probably due to the considerable attention because of the first fatal CCHF case from the mass media leading to a surge in “tickphobia,” but also to the information disseminated by Hellenic Center for Disease Control and Prevention regarding proper removal of attached ticks (Maltezou et al. 2009). However, tick populations might had really increased in 2008. Further, landscape changes, such as the construction of recreational parks, facilitate the establishment of tick populations close to human habitation, and increase the potential risk of being bitten, while the development of large suburban areas with private gardens provides an additional niche for arthropod vectors (e.g., ticks, mosquitoes, and biting flies) and peridomestic hosts (rodents) (Beugnet and Marie 2009).

Overall, a far as the zoonotic potential is concerned, it is highly important that almost all tick species recorded in the current survey are known vectors of many pathogenic agents and capable to transmit diseases to humans. Precisely, it was found that most ticks were adult female R. sanguineus (brown dog tick). This finding was not unusual, even though this tick shows higher preference to dogs than to humans, because R. sanguineus is among the most common tick species in pets, and its distribution and abundance in Meditteranean/Balkan area is high (Beugnet and Marie 2009). This tick species is considered the main vector of R. conorii. Dogs are the usual hosts of R. sanguineus; however, the real reservoir of R. conorii is still unknown, and wild rabbits, hares, hedgedogs, and rodents might play a role in its transmission (Rovery et al. 2008). Increased rickettsiosis cases were observed in Northeastern Greece in summer 2008 (based on our laboratory data); however, the exact number of cases is not known, as rickettsiosis cases might presented with a mild form and remain undetectable.

There are no former studies in Greece to compare the tick species feeding on humans, and it is not known whether the host-seeking and feeding behaviors of R. sanguineus were modified during the recent years. However, Parola et al. (2008) observed that the human affinity of R. sanguineus was increased in warmer temperatures, and that there is a warming-mediated increase in the aggressiveness of R. sanguineus, leading to increased human attacks, and they predicted that as a result of globalization and warming, more pathogens transmitted by the brown dog tick may emerge in the future. Actually, the temperature in spring and summer of 2007 in Greece was higher, and the rainfall was lower than usual, while the temperature reached record levels in June. Increased temperature levels were observed also in spring and summer of 2008, following a dry winter. These weather conditions might enable the xerophilus R. sanguineus to survive and increase its population, and to increase aggressiveness and the level of human attacks.

A recent study by Pavlidou et al. (2008) on 3249 ticks collected in 11 prefectures of Northern Greece during 2003–2006 showed that the most common tick (44.57%) was Ixodes ricinus, followed by R. bursa (19.15%) and H. marginatum (12.4%). However, ticks of that study were collected from domestic animals (mainly goats and sheep), which are not the preferable hosts of R. sanguineus, during spring and autumn in regions near oak and coniferous forests, facts that explain the high incidence of I. ricinus, which is an hygrophilus tick species adapted to cool weather. In the present study, the incidence of I. ricinus was low (1%) due to different season and weather conditions, and different host and habitat.

H. marginatum, a two-host tick and a main vector of CCHFV, accounted for 5.2% of the total number of studied ticks. This species parasitize mainly on cattle, and its activity peaks in spring and summer. A variety of factors, including climate, might play a role in CCHF emergence in Greece. However, no additional CCHF cases were observed, suggesting that the number of infected H. marginatum (as well as R. bursa, which also plays a role in CCHF epidemiology) was low. Studies to check the prevalence of CCHFV in ticks in Greece are in progress. R. annulatus accounted for 5% of the ticks. This tick species rarely bites humans, and up to now it is not associated with disease.

Prospective studies on ticks attached to humans are planned to relate data about tick's infection with probable human infection. The present study gives a first insight into the tick species parasitizing humans in Greece. As most of them are known vectors of various pathogenic agents, humans have to take personal protective measures to avoid tick exposure, and to be aware for prompt and proper tick removal, while tick control measures for livestock and pets are essential to eliminate the risk of tick-borne infections.