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Tick Bites on Humans in Southwestern Region of Turkey: Species Diversity/Turkiye'nin Guney Bati Bolgesinde Insanlardaki Kene Isiriklari: Turlerin Cesitliligi.

INTRODUCTION

Ticks are obligate ectoparasites and a variety of pathogens, including Rickettsia and other types of bacteria, viruses and protozoa can be transmitted to humans and domestic animals (1). Ticks can cause serious health problems in humans not only by the direct effects of ticks but also as vectors for many pathogens like Crimean-Congo hemorrhagic fever, Lyme disease, Tick-borne rickettsioses and Tularemia (2). Hitherto, a total of 907 tick species including Argasidae (n=186), Ixodidae (n=720) and Nuttalliella (n=1) were identified throughout the world. 267 out of them have been recognized as the transmitting vectors of diseases that are responsible for the health-related problems of humans (3). Ticks are widespread throughout Turkey (4) and thousands of people are affected every year by tick bites and tick-borne diseases (2,5). Up to present, a total of 47 tick species have been identified in Turkey and 31 of them have been found on humans (2). Ticks frequently found on humans in Turkey are Hyalomma marginatum, Hyalomma spp. immatures, Ixodes ricinus, Ixodes spp. immatures, and Rhipicephalus spp. (5,6).

Even though ticks have host-selectivity, they have an ability to feed on various hosts (7). It is reported that 267 tick species feed on humans (3). Furthermore, population of ticks and infestation rate of the hosts differ in a given region depending on seasonal fluctuations, land structure, vegetation and climatic change in tick population. (8,9). This study aimed to determine tick species feeding on humans and the environmental factors affecting tick-host interactions in the Southwestern Anatolia Region of Turkey.

METHODS

Characteristics of Study Area

The present study was carried out in nine different provinces located in two different geographical regions of Turkey (Figure 1). A total of 2.610 ticks were examined in this study. Of these ticks, 1.858 were collected from human in the Aegean Region (Afyon, Denizli, Izmir, Manisa, Mugla and Usak) and 752 from the Mediterranean Region (Antalya, Burdur, Isparta) of Turkey. The West Aegean Region (Denizli, Izmir, Manisa and Mugla province) has abundant superficial water resources and a mild Mediterranean climate with average temperatures of 8[degrees]C in winter and 28[degrees]C in summer. Additionally, a steppe climate is found in two neighboring provinces, namely Afyon and Usak, in inner Western Anatolia Region. On the other hand, Burdur and Isparta provinces in Mediterranean Region are located in an area with a series of shallow tectonic lakes within the folds of the Taurus Mountains in Southwestern Anatolia, Turkey. Antalya Province, which is located on the Mediterranean coast of south-west Turkey, between the Taurus Mountains and the Mediterranean sea has a hot-summer Mediterranean climate with hot and dry summers and mild and rainy winters.

Identification of ticks and Data Analysis

Between January and October 2007, ticks were collected from people applied to the city and/or town hospitals with complains of tick bites in nine different provinces of Turkey. Adult ticks were identified microscopically on the genus/species levels using related taxonomic keys (10,11). Also, stage of larvae and nymph were identified at the genus level, according to tick identification keys by Bakirci et al., (2017) (12). Data including species and developmental stages of all identified ticks were recorded. For the age analysis of the patients, eight groups were formed as age groups 0-6, 7-12, 13-18, 19-25, 26-40, 41-55, 56-65 and over 65. Also, the places where the hosts were bitten by the ticks, were divided into two groups, rural and urban. The chi-squared test was used to test for association among hosts bitten by identified ticks relative to variables like sex, age and origin.

Statistical Analyses

Analyses were performed with SPSS (SPSS Inc., Chicago, IL, USA, version 22.0) and P<0.05 was considered as statistically significant.

RESULTS

A total of 2.610 samples collected from humans were identified microscopically and identified tick species, their developmental stages and distribution between rural and urban areas are summarised in table 1. In the present study, 14 different tick species within seven genus were identified from human in nine different provinces of Turkey.

Obtained results showed that seven out of 2.610 ticks were (0.27 %) Argasidae (six Argas persicus and one Ornithodoros spp. nymph) and the remaining 2.603 were (99.73%) Ixodid.

Larvae (n=55) and nymphs (n=1.642) were identified at the genus level in 2.1 % and 62.9 % of the collected ticks, respectively. In addition to larvae and nymphs, some of the collected adult ticks have been identified at species level. Among these different developmental stages, the most prevalent species was Hyalomma spp. (78.79%), followed by Rhipicephalus spp. (18.94%), Ixodes spp. (0.88%), Dermacentor spp. (0.77%) and Haemaphysalis spp. (0.62%). Species like Ornithodoros spp. was detected in a single sample collected from Izmir province.

In the present study, ticks collected from human were mainly in the genus of Hyalomma and generally at its nymphal stage. Hyalomma spp. nymphs were most commonly detected in the Aegean (46.13%, n=1.204) and Mediterranean (14.48%, n=378) Regions. The prevalence of Hyalomma spp. nymph detected in Mugla was significantly higher than other provinces (P=0.000).

Hyalomma marginatum (n=233, 26.09%) was the most commonly identified species among the adult ticks. This was followed by R. bursa (n=228, 25.53%), R. turanicus (n=209, 23.41%), H. aegyptium (n=108, 12.10%), H. excavatum (n=35, 3.92%), H. anatolicum (n=21, 2.35%), D. marginatus (n=19, 2.13%), I. ricinus (n=13, 1.46%), R. sanguineus (n=13, 1.46%), Haemaphysalis parva (n=9, 1.00%), H. scupense (syn=H.detritum) (n=4, 0.45%) and H. rufipes (n=1, 0.11%) (Table 1). Hyalomma marginatum was detected in all provinces (Table 1). The highest infestation rate was found in Izmir (2.1%), while the infestation rate in Antalya (0.38%), Isparta (0.38%) and Burdur (0.49%) provinces was much lower. The prevalence of H. marginatum was statistically significant (P=0.000) among provinces.

Hyalomma excavatum was detected in all provinces, except Afyon. The prevalence of H. excavatum among provinces was statistically significant (p=0.000) and the highest prevalence was found in Usak (0.31%). Hyalomma rufipes was only detected in Izmir (Table 1).

The highest prevalence of R. turanicus (4%) and R. bursa (4.8%) was found in Mediterranean region (Antalya, Burdur and Isparta) with a statistically significant difference (P=0.000) among other regions. Rhipicephalus bursa and R. turanicus were seen most commonly in Antalya province. The highest infection rate of R. bursa was found in Antalya (2.95%), while the infection rate in Afyon (0.45 %), Denizli (0.34 %) and Usak (0.22 %) provinces was much lower. The prevalence of R. bursa among provinces was also statistically significant (P=0.000).

Ixodes ricinus was detected in Denizli, Izmir, Manisa, Mugla, Antalya and Burdur provinces with the highest prevalence detected in Mugla (0.19%). Nymphs and larvae of Ixodes spp. and nymphs and adults of D. marginatus were abundantly identified in Antalya province.

The data showing the locations of hosts bitten by ticks were further analyzed and the obtained results indicated that out of 2.610 samples, 1.546 were coming from rural areas including villages, farms, grasslands and picnic sites (59.23%), whereas 1.064 were from urban areas (40.77%).

Ticks were found mainly attached to human body and followed by extremities, head, inguinal region and other body regions with low infestation rate. Data gathered in the present study showed that Hyalomma spp. nymphs were the main ticks attaching human in all age groups (0-6, 7-12, 13-18, 19-25, 26-40, 41-55, 56-65 and over 65). Regarding other species of ticks described in the present study, the age of the host was to be significant. (Table 2).

DISCUSSION

Ticks are the most important vectors within pests following mosquitoes (13). The cost of the control of the ticks and tick-borne disease in all over the world is estimated to be between 13.9 and 18.7 million US dollars per year (14). In order to develop effective control measures for ticks and tick-borne diseases detailed epidemiological information on the distribution and seasonal activities of ticks in a particular region should be obtained (5). In previous studies focused on ticks of animals, 47 species of ticks from seven genera were identified in Turkey. Of the 47 different species of ticks, 38 species of six genera in the family Ixodidae, viz. Haemaphysalis, Hyalomma, Dermacentor, Rhipicephalus, Ixodes are of medical and veterinary importance (2,5).

In the present study, 14 different tick species within seven genus were collected from human (Table 1). It should be noted that tick species that feed on people living and/or vacationing in the Aegean (Afyon, Denizli, Manisa, Mugla and Usak) and Mediterranean (Antalya, Burdur, Isparta) regions are presented for the first time with this study. The current study showed that ticks biting on humans were mostly belonging to the genus Hyalomma and that nymphs of Hyalomma spp. was the most commonly encountered form in this genus (Table 1). These findings are in accordance with the previous studies performed on humans in which the majority of tick bites shown to be caused by nymphal form of the ticks (2,5). Furthermore, the prevalence of Hyalomma spp. nymph (71.2%) detected in the Aegean region was significantly higher compared to Mediterranean Region (P= 0.000). The genus Hyalomma (Koch, 1844), like all other tick species, has a great importance for human as well as animal health (15). Hyalomma marginatum is a characteristic species of steppe, savannah and lightly wooded hill and valley biotopes with fairly low humidity (16). In the present study, H. marginatum was found to be the most prevalent adult ticks collected on humans and the highest prevalence was detected in Aegean region. Obtained results in Aegean region were in parallel with the previous studies (4,5). The micro and macro habitat of the Aegean Region provides a good environment for this tick species.

In the present study the adult forms of H. aegyptium are also detected on humans. In general, the larvae and nymph forms of H. aegyptium feed on partridges, lizards and a wide variety of rodents and the adults feed on turtles (17). However, number of reports on human infestation by H. aegyptium are increasing (2,5,6). This fact is highlight the importance of H. aegyptium for both human and animal health as they are shown to be the vector of pathogens like Borrelia burgdorferi, Borrelia turcica, Theileria annulata, Pasteurella tularensis, Ricketsia aeschlimannii (18). It should be noted the presence of B. turcica, R. africae and R. aeschlimannii were shown in H. aegyptium and H. marginatum in Turkey in previous studies form (19,20).

This study was also indicated that Hyalomma spp. especially H. marginatum were detected more often in rural area than that in urban areas (Table 1). These findings are in accordance with the previous studies that H. marginatum adults which are known to be abundant in rural areas (10). Hyalomma rufipes, another tick species detected in the present study (only Izmir province), is a rare species and restricted in Aegean, Central and Marmara Regions of Turkey. However, Hyalomma rufipes was previously found on cattles in Manisa and Izmir provinces (20) and on horses in Bursa province (6). In Turkey, the first human infestation by H. rufipes which is believed to be the carrier of the Crimean-Congo hemorrhagic fever in Africa (21) was detected in Amasya province (22) where this disease is endemic (23).

The current study demonstrated that Rhipicephalus species were found to be the second most abundant ticks biting on humans, following Hyalomma species (Table 1). Data gathered in the present study, Rhipicephalus (Boophilus) annulatus species could not be determined on humans in all provinces, whereas was previously found on cattles in Burdur province (24) and on dogs in Antalya province (25). The unexistence of some species such as R. (B.) annulatus on human, could be explain with high host specificity and one-host biology (26). During the study, R. bursa was commonly found on humans, particularly in Antalya province (Table 1). Not only the present study but also the previous studies showed that R. bursa is one of the tick species often found on humans in Turkey (5,22). Rhipicephalus bursa and R. turanicus caused more biting cases in rural areas 67.54% and 65.07% respectively, whereas R. sanguineus caused more biting cases in urban areas (69.23%) (Table 1). The reason for this may be related to the fact that ticks of R. sanguineus are urban areas to support population of these ticks. On the other hand, R. bursa is a two-host species preferring ruminants (especially sheep), and its biology is mostly restricted to rural areas (10). It was indicated in previous studies that R. bursa carries several pathogens like R. aeschlimannii and CCHF (20,23).

There are 244 Ixodes species known to exist throughout the world. Among these, 63 species (26%) have been recorded as feeding on humans (3). In this study we encountered 13 Ixodes ricinus, nine Ixodes spp. nymphs and one Ixodes spp. larva (Table 1). Ixodes ricinus was previously found on sheep in Burdur province (24), on humans in Izmir province (27), on cattles in Manisa and Izmir province (14) and on goats in Antalya province (28). It is the main tick vector involved in the Tick-borne encephalitis virus (TBEV) infections in Europe (29). In addition, Anaplasma phagocytophilum was detected in cattle and sheep in the Middle and Eastern Black Sea Regions of Turkey where its potential vector, I. ricinus, is also widespread (30). The presence of A. phagocytophilum and R. monacensis was also demonstrated in I. ricinus collected from human in Turkey (20,30). Similar to Hyalomma spp., the proportion of I. ricinus bites in the present study was much higher in rural areas (84.61%) than that observed in urban areas (15.39%). The genus Dermacentor now has 35 species in the world. Notedly, it was demonstrated that 23 (66%) of the Dermacentor species have been feeding on humans. (3). In the present study, we encountered 19 adult D. marginatus and one Dermacentor spp. nymph on humans in all provinces except Denizli and Manisa province (Table 1). Dermacentor marginatus bite rate was also higher in rural areas in comparison to that observed in urban areas (68.42 % vs. 31.58%). Dermacentor marginatus is limited to areas with dense vegetation and trees in the Mediterranean region of Europe (10). It favours ecologically the areas under Oak and Pine plant cover. This situation would be an explanation, partly, why D. marginatus was not found in Denizli and Manisa provinces in which the ecology is not suitable for this tick species. Dermacentor marginatus was previously found on cattle, sheep and goats in Burdur province (24), on humans and cattle in Izmir province (14,27) and on goats in Antalya province (28). Dermacentor marginatus is a recognized vector for Coxiella burnetii, Rickettsia conori, R. slovaca, R. sibirica (16). Furthermore, the presence of R. raoultii was also demonstrated in D. marginatus collected from human in Turkey (20). It has been reported that R. raoultii species was previously detected in a D. marginatus that bite humans who developed TIBOLA/DEBONEL symptoms (20).

CONCLUSION

Taken together, the results obtained in the present study indicate that the prevalence and distribution of tick species on humans are common in the Aegean and Mediterranean regions where the study was conducted. The data suggest that tick species, especially H. marginatum, R. bursa, R. turanicus and H. aegyptium as well as nymphs of Hyalomma spp. can feed on humans more commonly than other tick species and developmental stages. The studies like the present one on monitoring of the tick bite exposure to human provide valuable information for determining the risk level of the tick borne diseases in a given area humans.

* Ethics

Ethics Committee Approval: In this study, ethical committee approval was not obtained due to the samples were taken from the patients who admit to some health facilities with complaining tick bites and sent to our department for identification.

Peer-review: Externally and internally peer-reviewed.

* Authorship Contributions

Surgical and Medical Practices: S.B., N.A., H.B.B., T.K., Concept: S.B., N.A., H.B.B., S.H., H.E., T.K., Design: S.B., N.A., H.B.B., S.H., H.E., T.K., Data Collection or Processing: S.B., N.A., S.H., T.K., Analysis or Interpretation: S.B., H.B.B., T.K., Literature Search: S.B., N.A., H.B.B., T.K., Writing: S.B.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.

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[iD] Serkan Bakirci, [iD] Nuran Aysul, [iD] Huseyin Bilgin Bilgic, [iD] Selin Hacilarlioglu, [iD] Hasan Eren, [iD] Tulin Karagenc

Aydin Adnan Menderes University Faculty of Veterinary, Department of Parasitology, Aydin, Turkiye

Cite this article as: Bakirci S, Aysul N, Bilgic H.B, Hacilarlioglu S, Eren H, Karagenc T, Tick Bites on Humans in Southwestern Region of Turkey: Species Diversity. Turkiye Parazitol Derg 2019;43(1):30-5.

Received/Gelis Tarihi: 30.11.2018 Accepted/Kabul Tarihi: 24.02.2019

Address for Correspondence/Yazar Adresi: Serkan Bakirci MD, Aydin Adnan Menderes University Faculty of Veterinary, Department of Parasitology, Aydin, Turkiye

Phone/Tel: +90 256 247 07 00 E-mail/E-Posta: serkanbakirci@adu.edu.tr ORCID ID: orcid.org/0000-0002-6033-2205

DOI: 10.4274/tpd.galenos.2019.6219
Table 1. Cases of tick bites by species, type of locality and provinces

Tick species       Type of locality Te Province
                   Rural    Urban    Afyon  Denizli  Izmir  Manisa

Hyalomma spp.       34       19       -       4        9      2
(larvae)
Hyalomma spp.      851      731      10     123      346    129
(nymphs)
Hyalomma spp.       14        -       -       -        6      1
(adults)
H. marginatum      164       69      32      20       55     20
H. aegyptium        73       35       3       8       31     12
H. excavatum        28        7       -       3        7      5
H. anatolicum       14        7       -       4        2      1
H. detritum          2        2       -       -        2      -
H. rufipes           1        -       -       -        1      -
Rhipicephalus        -        1       -       -        1      -
spp. (larvae)
Rhipicephalus       24       18       -       4       13      2
spp. (nymphs)
R. bursa           154       74      12       9       36     16
R. sanguineus        4        9       -       3        1      -
R. turanicus       136       73      11      14       30      7
Ixodes spp.          -        1       -       -        -      -
(larvae)
Ixodes spp.          5        4       -       1        1      -
(nymphs)
I. ricinus          11        2       -       1        2      1
Dermacentor spp.     -        1       -       -        1      -
(nymphs)
D. marginatus       13        6       2       -        2      -
Haemaphysalis        4        3       -       1        2      -
spp. (nymphs)
H. parva             9        -       2       2        1      -
Argas persicus       4        2       1       -        2      1
Ornithodoros spp.    1        -       -       -        1      -
(nymphs)
Total                1.546    1.064  73     197      552    197

Tick species       Type of locality Te Province
                   Mugla  Usak  Antalya  Burdur  Isparta  P value

Hyalomma spp.       26      4     6       2        -
(larvae)
Hyalomma spp.      528     68   298      25       55      0.000 (*)
(nymphs)
Hyalomma spp.        -      1     3       3        -
(adults)
H. marginatum       51     22    10      13       10      0.000 (*)
H. aegyptium        16      7    17       3       11
H. excavatum         4      8     2       4        2      0.000 (*)
H. anatolicum        -      9     -       2        3
H. detritum          -      -     1       -        1
H. rufipes           -      -     -       -        -
Rhipicephalus        -      -     -       -        -
spp. (larvae)
Rhipicephalus        4      4    14       -        1
spp. (nymphs)
R. bursa            23      6    77      27       22      0.000 (*)
R. sanguineus        4      -     5       -        -
R. turanicus        31     11    80      10       15      0.000 (*)
Ixodes spp.          -      -     1       -        -
(larvae)
Ixodes spp.          -      -     7       -        -
(nymphs)
I. ricinus           5      -     3       1        -
Dermacentor spp.     -      -     -       -        -
(nymphs)
D. marginatus        2      2     6       3        2
Haemaphysalis        -      -     2       1        1
spp. (nymphs)
H. parva             -      1     1       2        -
Argas persicus       1      1     -       -        -
Ornithodoros spp.    -      -     -       -        -
(nymphs)
Total              695    144   533      96      123

(*) statistically significant (P<0.05) based on the Chi-square test

Table 2. Distribution of ticks based on the ages of the humans

Genera                                   Age groups
                                    0-6  7-12  13-18  19-25  26-40

Hyalomma spp. (adults)               36   24    29     33    105
Hyalomma spp. (nymph, larvae)       452  222   112    117    274
Rhipicephalus spp. (adults)         107   61    18     28     72
Rhipicephalus spp. (nymph, larvae)   24   11     -      2      -
Dermacentor marginatus                5    3     3      -      3
Dermacentor spp. (nymph)              -    -     -      -      1
Ixodes ricinus                        3    -     2      -      4
Ixodes spp. (nymph, larvae)           4    4     1      -      -
Haemaphysalis parva                   3    1     -      1      -
Haemaphysalis spp. (nymph)            6    -     -      1      -
Argas persicus                        1    -     -      1      2
Ornithodoros spp. (nymph)             -    -     -      -      -
Total                               641  326   165    183    461

Genera                                                     Total
                                    41-55  56-65  65-over

Hyalomma spp. (adults)              104     53     32        416
Hyalomma spp. (nymph, larvae)       241    120     97      1.635
Rhipicephalus spp. (adults)          82     50     32        450
Rhipicephalus spp. (nymph, larvae)    4      -      2         43
Dermacentor marginatus                2      -      3         19
Dermacentor spp. (nymph)              -      -      -          1
Ixodes ricinus                        1      1      2         13
Ixodes spp. (nymph, larvae)           -      1      -         10
Haemaphysalis parva                   1      1      2          9
Haemaphysalis spp. (nymph)            -      -      -          7
Argas persicus                        1      1      -          6
Ornithodoros spp. (nymph)             1      -      -          1
Total                               437    227    170      2.610
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Title Annotation:Original Investigation/Ozgun Arastirma
Author:Bakirci, Serkan; Aysul, Nuran; Bilgic, Huseyin Bilgin; Hacilarlioglu, Selin; Eren, Hasan; Karagenc,
Publication:Turkish Journal of Parasitology
Article Type:Report
Geographic Code:7TURK
Date:Mar 1, 2019
Words:4417
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