Introduction

Ticks are among the most common human ectoparasites. Their bites are usually painless; therefore many people may not be aware of their bites. Ticks may be responsible for transmission of numerous viral, rickettsial, bacterial and protozoan disease agents (Estrada-Peña and Jongejan 1999; Otranto et al. 2014). Irritation, allergic reactions, and rarely paralysis are other problems associated with tick bites (Jongejan and Uilenberg 2004).

Ticks are common throughout Turkey (Merdivenci 1969; Bursali et al. 2012) and thousands of people are affected by tick bites and tick-borne diseases in Turkey every year (Vatansever et al. 2008; Gargili et al. 2011; Bursali et al. 2013; Bakirci et al. 2014). Crimean-Congo hemorrhagic fever (CCHF), tularemia and rickettsiosis are some of the tick-borne diseases seen in Turkey (Tonbak et al. 2006; Yesilyurt et al. 2011; Kuloglu et al. 2012). Since 2002, when the CCHF was first detected, thousands of CCHF cases have been reported in Turkey. According to The Republic of Turkey Ministry of Health, between 2002 and December 2014, 9046 CCHF cases and 440 deaths were documented in Turkey.

To date, more than 700 hard tick species have been described throughout the world, 269 of which have been recognized as the cause of health-related problems for humans (Guglielmone et al. 2014; Apanaskevich and Apanaskevich 2015a, b). Turkish tick fauna currently consist of 47 tick species and 31 of them have been found on humans (Bursali et al. 2012; Keskin et al. 2014). It is known that collection and accurate identification of ticks is an essential step for further studies about ticks and tick-borne diseases (Marrelli et al. 2007; Estrada-Peña et al. 2013). Although few quantitative studies about ticks infesting human have been documented in several provinces (Vatansever et al. 2008; Gargili et al. 2011; Bursali et al. 2013; Bakirci et al. 2014), there is limited information on this issue in large parts of Turkey.

To the best of our knowledge, this study is the first detailed investigation on ticks infesting humans in Corum and Yozgat provinces, except individual or incidental records. The aim of this study is to determine the species composition of ticks infesting humans in Corum and Yozgat provinces. We believe that this study will provide useful information on ticks and tick-borne diseases for those interested.

Materials and methods

Study area

The study was conducted in 2 neighbor provinces (Fig. 1) of Turkey. Corum province (40°33′00″ N, 34°57′14″ E) is situated on Middle Black Sea in Black Sea Region and divided into 14 districts (see Fig. 1). The climate of Corum province is mainly steppe, but Kargi, Osmancik, Iskilip, Lacin, Dodurga, Oguzlar and Bayat districts are under the influence of oceanic climate. Forests cover about 28 % of the province. The province covers 12,820 km2 areas. The mean altitude is 801 m and the mean annual precipitation is 429 mm. At present, approximately 527 thousand people live in the province; 71 % person lives in urban, 29 % person lives in rural areas.

Fig. 1
figure 1

Map of the study area, Corum and Yozgat provinces, Turkey

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Yozgat province (39°49′15″ N, 34°48′30″ E) is located in the Middle Kızılırmak Basin in the Central Anatolia Region. Yozgat province has 14 districts (see Fig. 1). The main climate of Yozgat province is continental, but the oceanic climate is seen in some regions. The predominant vegetation of Yozgat province is steppe and forests cover just about 9 % of the province. The province covers an area of 14123 km2. The mean altitude is 1418 m and the mean annual precipitation is 554 mm. At present, approximately 450 thousand people live in the province; 59 % person lives in urban, 41 % person lives in rural areas.

Ticks collection and morphological identification

Between June and September 2009, ticks were collected on humans by doctors, nurses, or health technicians under aseptic conditions in the major hospitals and local health clinics of Corum and Yozgat provinces and stored in 70 % alcohol. Afterward, ticks were deposited in the Acarology laboratory in Gaziosmanpasa University (Tokat, Turkey) for taxonomic identification. Tick samples were identified to species under the stereomicroscope (Leica MZ16, Germany). The adult ticks were identified using the morphological keys of Filippova (1977, 1997), Walker et al. (2000) and Estrada-Peña et al. (2004), while the immature ticks were identified using keys and descriptions by Filippova (1977, 1997) and Apanaskevich and Horak (2008).

Results

In total, 2110 ticks representing 14 different species were collected on 2085 humans in Corum and Yozgat provinces, between June and September 2009. Of those, 1551 (687♂, 450♀, 407 nymphs, 7 larvae) were collected from Corum province while 559 (330♂, 180♀, 49 nymphs) were collected from Yozgat province. Twelve tick species were identified in Corum province (Table 1), whereas 10 tick species were identified in Yozgat province (Table 2). The most prevalent ticks infesting humans in both provinces were Hyalomma marginatum, Dermacentor marginatus and Rhipicephalus turanicus sensu lato. Haemaphysalis erinacei taurica, Haemaphysalis sulcata, Ixodes laguri and Ixodes ricinus were only found in the Corum province while Rhipicephalus annulatus and Rhipicephalus sanguineus sensu lato were only found in the Yozgat province. Additionally, a total of 386 immature Hyalomma were found on humans in Corum (335 nymphs, 7 larvae) and Yozgat provinces (44 nymphs). In addition I. laguri and H. e. taurica was recorded for the first time in Corum province.

Table 1 Ticks infesting humans in Corum province and its districts
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Table 2 Ticks infesting humans in Yozgat province and its districts
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Tick infestations on humans were seen in all district (except Bogazkale) of the Corum province, whereas tick infestations on humans in the Yozgat province were seen only in 8 district, namely Akdagmadeni, Bogazliyan, Cayiralan, Kadisehri, Saraykent, Sarikaya, Sorgun, and Sefaatli. The prevalence of tick infestation in Corum province was found highest in Capital district (n = 439), Mecitozu (n = 266), Sungurlu (n = 176), Osmancik (n = 166) and Alaca (n = 140) districts while the prevalence of tick infestation in Yozgat province was found highest in Sorgun (n = 266) and Akdagmadeni (n = 180) districts. Distributions of ticks on humans according to the district are shown in Table 1 (Corum) and Table 2 (Yozgat) for each tick species.

Discussions

Although tick-borne human diseases, especially CCHF, are seen commonly in Corum and Yozgat provinces (Tanir et al. 2009; Kandis et al., 2012), information on ticks infesting humans are very scanty in these provinces. In the present study, a total of 2110 hard ticks were collected from humans in the Corum and Yozgat provinces between June and September 2009. The results obtained in this study showed that at least 14 different hard tick species (12 species from Corum, 10 species from Yozgat) were found feeding on humans in the study area.

The species H. marginatum was most prevalent ticks collected on humans, as similarly with other studies (Bursali et al. 2012, 2013; Bakirci et al. 2014). The tick is the main vector of CCHF in Turkey (Tonbak et al. 2006; Vatansever et al. 2007; Tekin et al. 2012). In addition, several tick-borne pathogens such as Rickettsia aeschlimannii and Borrelia burgdorferi sensu stricto have been isolated from H. marginatum in Turkey (Gargili et al. 2012; Orkun et al. 2014). Other encountered hyalommids infesting humans in the both provinces were identified as Hyalomma aegyptium and Hyalomma excavatum. H. aegyptium is a specific parasite of the tortoise, while H. excavatum parasitize many kinds of livestock, preferring cattle. There are many reports of human infestations by both species in Turkey (Vatansever et al. 2008; Karaer et al. 2011; Bakirci et al. 2014). Rickettsia africae and R. aeschlimannii in H. aegyptium; R. aeschlimannii and B. burgdorferi sensu stricto in H. excavatum have been detected in Turkey (Gargili et al. 2012; Orkun et al. 2014). However, there is no sufficient evidence on the vector competence of these tick species in Turkey. Immature Hyalomma have been also collected on humans in this study. It is well–known that morphological identification of immature Hyalomma is very difficult (Apanaskevich and Horak 2008; Hagman et al. 2014); therefore identifications of these specimens should be confirmed by a molecular approach in further studies.

The genus Dermacentor currently consists of 38 species distributed in the Palearctic and Nearctic Regions (Apanaskevich and Bermúdez 2013; Guglielmone et al. 2014; Apanaskevich and Apanaskevich 2015a, 2015b). Among the member of genus Dermacentor, 25 species can feed on humans (Guglielmone et al. 2014; Apanaskevich and Apanaskevich 2015a, 2015b). For a long time, there are many disagreements about the identification of Palearctic Dermacentor. Filippova and Plaksina (2005) have emphasized that species identifications of Dermacentor marginatus complex are very difficult. Without any molecular study, identification of immature ticks is difficult as species level and their identification are generally identified in genus level. However, Filippova (1997) provide many useful morphological characters for identification of immature Dermacentor ticks. Based on Filippova (1997), nymphs of D. marginatus can be distinguished from other Dermacentor nymphs by a combination of the second palpal segment about half as long again as that of third when viewed ventrally, on the scutum less than 40 short setae, spur of coxa IV is usually shorter than III. Nowadays, genus Dermacentor is under revision and, therefore it expects that some changes in the taxonomy and nomenclature of this genus in the near future (Guglielmone et al. 2014).

In the present study, D. marginatus was second abundant tick species infesting humans in Corum and Yozgat provinces. D. marginatus is typically three-host ticks and occurs widely in West/Southwest Palaearctic region (Estrada-Peña et al. 2004). The tick is an important vector of Coxiella burnetii, Rickettsia conorii, Rickettsia slovaca and Rickettsia sibirica (Farkas et al. 2013). The immature of D. marginatus feed on small mammals and rarely Anura, Aves and Squamata (Farkas et al. 2013; Guglielmone et al. 2014). Several tick-borne pathogens such as Rickettsia raoultii, R. slovaca, and CCHF have been detected in D. marginatus (Albayrak et al. 2010; Gargili et al. 2012; Orkun et al. 2014). Although numerous cases of human infestations by D. marginatus have been reported in Turkey (Gargili et al. 2010; Karaer et al. 2011; Bursali et al. 2013; Bakirci et al. 2014), sufficient evidence has not been found about that D. marginatus may play a role in transmission of these pathogen.

The genus Haemaphysalis is represented 167 species in the world and 56 of them can be infested on humans (Guglielmone et al. 2014). Haemaphysalis parva and Haemaphysalis punctata are two of very common haemaphysalids ticks infesting humans (Karaer et al. 2011; Bursali et al. 2011). In the present study, H. parva and H. punctata were collected from both Corum and Yozgat provinces, whereas H. sulcata was collected only Corum province. Although several tick-borne pathogens such as B. burgdorferi sensu stricto Rickettsia hoogstraalii, CCHFV have been detected in H. parva (Gunes et al. 2011; Orkun et al. 2014), there is limited information on vectorial capacity of the tick.

Two species belonging to the genus Ixodes were only collected on humans only in Corum province in the current study. I. ricinus is one of the most common tick species in Turkey (Merdivenci 1969; Bursali et al. 2012). This tick is a vector of many important pathogens that cause diseases in humans including Lyme disease, anaplasmosis and babesiosis (Carpi et al. 2011; Lommano et al. 2012). In Turkey, B. burgdorferi sensu lato, Rickettsia monacensis, Rickettsia helvetica and CCHF virus are some of the tick-borne pathogens reported in I. ricinus (Guner et al. 2003; Albayrak et al. 2010; Gargili et al. 2012). On the other hand, information on the distribution of I. laguri in Turkey is very scanty. Main hosts of the tick are rodents (Balashov 1997). This tick was formerly found on Arvicola amphibius (as Arvicola terrestris hintoni), Spermophilus citellus (as Citellus citellus), Crocidura sp., Microtus sp., Meriones tristrami (as Meriones blackeri intraponticus) by Arthur (1957) and Merdivenci (1969) in Turkey. Subsequently, the presence of I. laguri on animals and humans were reported in several studies (Bursali et al. 2012, 2015). We believe that the distribution area of I. laguri is expected to expand in Turkey with additional investigations.

Rhipicephalus bursa and R. turanicus sensu lato were collected on humans in Corum while R. annulatus, R. bursa, R. turanicus sensu lato and R. sanguineus sensu lato were collected on humans in Yozgat province. Rhipicephalus sanguineus complex is composed of at least 12 different species, with probable cryptic species and there are many taxonomic problems in morphological identification of members of R. sanguineus complex (Guglielmone et al. 2014; Nava et al. 2015). The type specimen of R. sanguineus sensu stricto has been lost and the original description given by Latreille was poor (Dantas-Torres et al. 2013; Guglielmone et al. 2014; Nava et al. 2015). The taxonomic status of R. sanguineus sensu stricto is still unclear. Guglielmone et al. (2014) stated that all records (except Gallia) of R. sanguineus sensu stricto from around the world are currently speculative. Nava et al. (2015) highlighted that “R. sanguineus species group” or “R. sanguineus sensu lato” should be used instead of “R. sanguineus sensu stricto” until the taxonomic status of this species is clarified. In this study, a female of R. sanguineus sensu lato was collected from human only in Yozgat province. This species is associated with several zoonotic diseases, which is one of them Mediterranean Spotted Fever (MSF). Although human infestations by the R. sanguineus sensu lato are rarely reported (Bursali et al. 2011, 2013; Bakirci et al. 2014), many MSF cases have been reported in Turkey, especially Thrace region (Kuloglu et al. 2012).

During the study, R. turanicus sensu lato were commonly found on humans, particularly in Corum province. There is continuing debate about the taxonomic status of this species. Guglielmone et al. (2014) have emphasized that usage of epithet turanicus to any populations (except identified in Filippova 1997) will not be possible until the taxonomic status of this species is clarified. In the present study, we were used key provided by Filippova (1997) for the identification of R. turanicus. Nonetheless, we prefer to use of “R. turanicus sensu lato” instead of “R. turanicus sensu stricto” to avoid conflicting views about this taxon (as proposed by Guglielmone et al. 2014). R. turanicus sensu lato can feed on a wide variety of hosts, including hedgehogs, hares, cattle, sheep, goats, and domestic dogs (Walker et al. 2000). Although there are many reports of human infestations by R. turanicus sensu lato (Karaer et al. 2011; Bursali et al. 2012; Bakirci et al. 2014), information about its vectorial capacity is very limited.

R. bursa is one of the tick species commonly found on humans in Turkey (Gargili et al. 2010; Bursali et al. 2011; Bakirci et al. 2014; Orkun et al. 2014). The tick is a highly distinctive species; it can be easily identified from densely punctate scutum or conscutum. Several pathogens such as R. aeschlimannii and CCHF have been detected in R. bursa tick (Gargili et al. 2012; Tekin et al. 2012). According to current data, the role of R. bursa in the transmission of these pathogenic agents to humans in Turkey is still unclear. On the other hand, human infestations by R. annulatus ticks are very rare (Bursali et al. 2011; Bakirci et al. 2014). R. annulatus is a one–host tick and all parasitic stage of the tick mainly feed on cattle, therefore human infestations by the tick are incidental.