J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 252 http://jad.tums.ac.ir Published Online: September 30, 2018 Original Article Tick Ectoparasites of Animals in Borderline of Iran-Iraq and Their Role on Disease Transmission Omid Banafshi 1, 2, Ahmad Ali Hanafi-Bojd 2, Mohamad Karimi 1, Faezeh Faghihi 3, Mojtaba Beik-Mohammadi 4, Sahere Gholami 2, Siavash Javaherizadeh 5, Hamideh Edalat 2, *Hassan Vatandoost 2, *Zakkyeh Telmadarraiy 2 1Zoonoses Research Center, Kurdistan University of Medical Sciences, Sanandaj, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3Cellular and Molecular Research Center, Iran University of Medical Sciences, Tehran, Iran 4Department of Medical Entomology and Vector Control, Faculty of Health, Urmia University of Medical Sciences, Urmia, Iran 5Faculty of Paramedical Science, Clinical Laboratory Science, Islamic Azad University, Tehran Medical Branch, Tehran, Iran (Received 21 May 2017; accepted 23 June 2018) Abstract Background: Since ticks are potent vectors of various diseases, identification of these species are clinically im- portant to protect the public health and control veterinary problems in the communities. We aimed to figure out the frequency of ticks on cows, goats, sheep, lambs, turtles and also obscure hosts in Kurdistan Province, bordered with Iraq June 2012 to May 2013. Methods: The hosts were selected randomly and examined individually for tick infestation. In case of infestation, ticks were collected using forceps and then preserved in 70% ethyl alcohol. All collected specimens were preserved in tubes and relative information was recorded and then identified based on morphological characteristics. Results: Totally, 1209 ticks were collected. The prevalence of ticks on cows, sheep, goats, lambs, turtles, poultry and obscure hosts was 11.33%, 55.41%, 6.53%, 5.95%, 0.9%, 8.02% and 11.82% respectively. The mean number of ticks on each animal was 1.6. Number of 5 genera, including Rhipicephalus, Argas, Ornithodoros, Hyalomma and Haem- aphysalis and 9 species; including R. sanguineus (60.05%), R. bursa (0.08), Hy. anatolicum (12.33), Hy. asiaticum (1.49), Hy. aegyptium (0.91), Hy. marginatum (0.08), Haemaphysalis parva (4.22), Hyalomma sp. (0.99), Orni- thodoros lahorensis (11.83), and Argas persicus (8.02) were identified. Conclusion: The most abundant species in this study area was Rh. sanguineus (60.05%). Due to high prevalence of tick specimens and a variety of collected species from sheep (55.41%), the vaccination of sheep and control of tick vectors are recommended. Keywords: Tick, Ruminants, Turtle, Iran Introduction Ticks (Acari: Ixodidae) are considered as the important vectors of pathogens (1). They play an important role in the survival of the pathogens that cause disease in humans and animals (2). Ticks are able to transmit a vari- ety of pathogens that are responsible to de- velop some diseases such as tick-borne en- cephalitis, Crimean Congo Hemorrhagic Fe- ver (CCHF), anaplasmosis, babesiosis, rick- ettsiosis, borreliosis and ehrlichiosis (3, 4). Such diseases are considered as public health or veterinary problems in the countries (5, 6). To the best of our knowledge, 10% of the cur- rently known tick species act as vectors of path- ogens of animals and humans (2). In addition to the transmission of pathogens, they are also responsible for damages directly due to their feeding behavior (7). As only 10% of tick spe- cies transmit a number of pathogens, identifi- cation of tick species is important. Tick spe- *Corresponding authors: Dr Hassan Vatandoost, E- mail: hvatandoost1@yahoo.com, Dr Zakkyeh Telma- darraiy, E-mail: telmadarraiy@tums.ac.ir http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 253 http://jad.tums.ac.ir Published Online: September 30, 2018 cies distribution in Iran is briefly investigated on the basis of published records. data were presented for 642 ixodid ticks taken from small-sized mammals, mainly rodents in dif- ferent zoogeographical zones of Iran (8). The prevalence of ixodid ticks was studied on cattle in Mazandaran Province, north of Iran (9) and east of the country (10) in another study the prevalence of ticks was investigated in Khuzestan Province and showed Shosh was the most infected city in Khuzestan, Ticks infection rate on sheep, goat, and cow was 84.12%, 12.69% and 3.17%, respectively (11). In a similar investigation, the distribution and ecological preferences of ticks of domestic animals were studied from 2002 to 2005 in north part of the country (12). The prevalence of ticks was surveyed in north-west of the country in Ardebil (13) and West Azerbaijan (14). Additionally, hard ticks of domestic ru- minants were surveyed in central part of Iran (15). Recently, some other investigations have been carried out in some other geographical locations of Iran (16-19), and in Kurdistan region of Iran and Iraq (20-22). In 2002, the presence of Hy. aegyptium from Testudo grae- ca turtle was reported in Iran (23). Hy. ae- gyptium and T. graeca were found in north- west of Iran (24). Recently the situation of tick born disease showed in Iran. The CCHFV RNA was detected in 5.2% of 492 ticks col- lected from livestock in different regions of Golpayegan (6). In total, 49 ticks including five species: R. sanguineus, Hyalomma ana- tolicum, Hy. asiaticum, Hy. dromedarii and Hy. marginatum with a prevalence of 46.9%, 32.7%, 4.1%, 4.1% and 2.1% respectively were identified; and CCHFV was detected in three ticks among 49 collected ticks. The ticks infected with CCHFV belonged to the genus Hyalomma and Rhipicephalus. Phylogenetic analysis demonstrated that two sequences clus- tered in clade IV (Asia-1) and one sequence was located within clade IV (Asia-2) (25). All positive ticks were from Hyalomma genus and Hy. marginatum species. They were not able to find virus in Hy. anatolicum, Hy. schulzei, Hy. dromedarii, R. sanguineus and Argas per- sicus. Hyalomma marginatum is the main vec- tor in that study (26) Despite the aforementioned investigations, there still seems to be a gap in our knowledge about distribution of tick species in Iran. This study was aimed to figure out the frequency of ticks on cows, goats, sheep, lambs, turtles and also obscure hosts in Kurdistan Province, bordered with Iraq. Materials and Methods This survey was carried out in Kurdistan Province, located in west part of Iran, in Re- gion 3 and bound by Iraq on the west, the province of West Azerbaijan to its north, Zan- jan to the northeast, Hamedan to the east and Kermanshah to the south (27). This province is one of the 31 provinces of Iran. It is 28817km² in area (Coordinates: 35.3113°N 46.9960°E). The capital of Kurdistan Province is the city of Sanandaj, located in Sanandaj County. Other counties with their major cities are Ma- rivan, Baneh, Saqqez, Qorveh, Bijar, Ka- myaran, Dehgolan, Diwandarreh and Sarva- bad (Fig. 1). Samples collection From June 2012 to May 2013, ticks from goats, cows, sheep, lambs, turtles and obscure hosts from various regions of the province were collected. Ticks were mostly found on sheep of the livestock. In total, 724 animals from 104 herds including 62 cows, 506 sheep, 73 goats and 23 lambs were selected randomly and examined individually for tick infesta- tion. Additionally, we selected 2 turtles and 37 obscure hosts randomly for detection of tick infestation on them. Thirty minutes were spent for each flock to collect ticks. All in- spections and tick collections were carried out between 08:00 a.m. and 11:00 a.m. In case of infestation, ticks were collected using forceps and then preserved in 70% ethyl alcohol. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 254 http://jad.tums.ac.ir Published Online: September 30, 2018 Collected samples were preserved in tubes and relative information was recorded such as collector name, date, host information and date of collection, then, samples were trans- ferred to the Entomology Laboratory, School of Public Health, Tehran University of Med- ical Sciences, Tehran, Iran. All collected sam- ples were identified based on morphological characteristics and the keys given by Janbakhsh (28) and Walker et al. (29) based on shape of capitulum, scutum, eyes, festooned and hypo- stome, spiracle, genital groove, spure of coxa, adanal shield and other appropriate characters. Results Totally 1209 ticks were collected and the occurrence of ticks on cows, sheep, goats, lambs, turtles, poultry and obscure hosts was 11.33%, 55.41%, 6.53%, 5.95%, 0.9%, 8.02% and 11.82% respectively. The mean number of ticks on each animal was 1.6 ticks per an- imal. Totally 5 Genus: Rhipicephalus, Argas, Ornithodoros, Hyalomma and Haemaphysalis were identified in study areas (Table 1). Rhip- icephalus sanguineus was the most abundant species in the studied area (60.05%), also, we found R. bursa (0.08%), Argas persicus (8.02 %), Ornithodoros lahorensis (11.83%), Hy. marginatum (0.08%), Hy. asiaticum (1.49%), Hy. anatolicum (12.33%), Hy. aegyptium (0.91 %), Ha. parva (4.22%) and Hyalomma sp. (0.99%). Spatial distribution of tick species in different elevations is presented in Fig. 2. The coordinates of collection sites have presented in Table 2. Fig. 1. The study area, Kurdistan Province is located in west part of Iran http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 255 http://jad.tums.ac.ir Published Online: September 30, 2018 Table 1. Tick species and their hosts and places in Kurdistan Province, 2012–2013 (N: Nymphs, F: Females, M: Males) Species of ticks Host and Place (%) Collected samples Total (%) Cow Sheep Goat Lamb Turtle Poultry Fold N F M R. sanguineus 17 572 65 72 0 0 0 53 200 473 726 (60.05) R. bursa 0 1 0 0 0 0 0 0 0 1 1 (0.08) Hy. anatolicum 114 35 0 0 0 0 0 0 88 61 149 (12.33) Hy. asiaticum 0 5 13 0 0 0 0 0 6 12 18 (1.49) Hy. aegyptium 0 0 0 0 11 0 0 0 9 2 11 (0.91) Hy. marginatum 0 0 1 0 0 0 0 0 0 1 1 (0.08) H. parva 0 51 0 0 0 0 0 0 20 31 51 (4.22) Hy. sp 6 6 0 0 0 0 0 1 11 0 12 (0.99) O. lahorensis 0 0 0 0 0 0 143 122 8 13 143 (11.83) A. persicus 0 0 0 0 0 97 0 63 21 13 97 (8.02) Total 137 (11.33) 670 (55.41) 79 (6.53) 72 (5.95) 11 (0.90) 97 (8.02) 143 (11.82) 239 (19.77) 363 (30.02) 607 (50.21) 1209 (100) Fig. 2. Spatial distribution of livestock ticks in different altitudinal categories of Kurdistan Province of Iran, 2012- 2013 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 256 http://jad.tums.ac.ir Published Online: September 30, 2018 Table 2. Spatial distribution of ticks collected from the study area, Kurdistan Province of Iran, 2012–2013 (+: Collected,-: Not collected) County Village X Y Host Hy. aegyptium Rh. sanguineus Hy. anatolicum Hy.asiaticum R.bursa O. lahorensis Ha.parva Bijar Khorkhore 47.1094 35.3086 Sheep - + - - - - - Bijar Sabzevar 47.5833 35.7 Sheep - + + - - - - Bijar Bijar-salavatabad 47.55 36.0166 Sheep - + - - - - - Bijar Salavatabad 47.55 36.0166 Cow - - + - - - - Bijar Salavatabad 47.55 36.0166 Cow - - + - - - - Bijar Salavatabad 47.55 36.0166 Goat - + - - - - - Bijar Top aghach 47.8161 36.0508 Sheep - - - - - + - Bijar Top aghach 47.8161 36.0508 Sheep - - - - - + - Qorveh qaleh 47.4810 35.0803 sheep - + - - - - - Qorveh Maloj 47.9733 35.2922 sheep - - + - - - - Qorveh Kaniganji 47.3611 35.1332 Sheep - - - + - - - Qorveh Kaniganji 47.3611 35.1332 Sheep - + - - - - - Qorveh Qorveh 47.7951 35.1594 Goat - - + + - - - Qorveh Qorveh 47.7951 35.1594 Sheep - - - - - - - Qorveh Malvjh 47.9733 35.2922 Goat - - - - - + - Qorveh Nazem Abad 47.9625 35.1038 Sheep -Goat - - - - - - + Qorveh Nazem Abad 47.9625 35.1038 Sheep -Goat - - - - - + - Qorveh Nazem Abad 47.9625 35.1038 Sheep -Goat - + - - - - - Qorveh Shirvaneh 47.8755 34.9566 Goat - - - - - + - Sanandaj Ali jan 46.6833 35.9166 Sheep - + - - - - - Sanandaj Doseh 46.8955 35.4566 sheep - + - - - - - Sanandaj qolyan 47.0106 35.2355 sheep - - + - - - - Saqez Saqez 46.2892 36.2523 Turtle + - - - - - - Saqez Eslam Abad 46.7666 36.3666 Sheep - - + - - - - Sarvabad Anjameh 46.35 35.3666 Goat - + - - - - - Sarvabad Anjameh 46.35 35.3666 Cow - + - - - - - Sarvabad Bandul 46.1535 35.1911 Sheep - + - - - - - http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 257 http://jad.tums.ac.ir Published Online: September 30, 2018 Sarvabad Doroud 46.3533 35.2994 Sheep /♀ - + - - - - - Sarvabad Doroud 46.3533 35.2994 lamb/ ♀ - + - - - - - Sarvabad Hezarkhani 46.3666 35.35 Sheep /♀ - + - - + - - Sarvabad Hezarkhani 46.3666 35.35 Sheep /♀ - + - - - - - Sarvabad Hezarkhani 46.3666 35.35 Goat /♀ - + - - - - - Sarvabad Hezarkhani 46.3666 35.35 lamb/ ♀ - + - - - - - Sarvabad Nasl 46.4333 35.3 Sheep /♀ - + - - - - - Sarvabad Nasl 46.4333 35.3 Sheep /♀ - + - - - - - Sarvabad Nasl 46.4333 35.3 sheep /♂ - + - - - - - Sarvabad Nasl 46.4333 35.3 Cow/ ♀ - + - - - - - Sarvabad Nasl 46.4333 35.3 Sheep - + - - - - - Sarvabad Nasl 46.4333 35.3 Sheep /♀ - + - - - - - Table 2. Continued … http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 258 http://jad.tums.ac.ir Published Online: September 30, 2018 Discussion Ticks are considered as ectoparasites, liv- ing by hematophagy on the blood of mammals, birds, and sometimes reptiles and amphibians. About 10% of Ixodidae (hard ticks) and Ar- gasidae (soft ticks) are vectors of a number of diseases that affect both humans and other animals. As ticks are important vectors of dis- eases; they are subject of many studies in Iran. Due to former investigations, there is limited information about distribution of tick infesta- tion in Kurdistan Province. In most regions of Iran, the dominant tick genera responsible for infestation belong to Hy- alomma, Rhipicephalus, Haemaphysalis, and Ixodes (30). In this investigation, we could collect three of the aforementioned genera except for Ixodes but also we collected some species of genera Argas and Ornithodoros too. We collected 1209 ticks. Most of the col- lected ticks were male (50.21%) (Table 1). Our survey revealed that the most occurrenc- es of ticks were observed on sheep (55.41%). The identification of collected ticks also re- vealed that the occurrence of ticks on cows, goats, lambs, turtles and obscure hosts were 11.33%, 6.53%, 5.95%, 0.9% and 11.82% re- spectively. As haemoparasitic diseases are con- sidered as a major problem to efficient sheep production in Iran due to theileriosis and babesiosis, it has important role (30). The ma- jor tick genera found on sheep and goats are mostly Hyalomma, Rhipicephalus, Haemaphy- salis and Ixodes (30). Our investigation re- vealed the presence of all species of ticks ex- cept Hy. marginatum and Hy. aegyptium on sheep. Due to high prevalence of tick speci- mens and variety of collected species of sheep, the vaccination of sheep and control of tick vectors are recommended. An investigation in Kurdistan region in Iraq was carried out (22). Three genera spe- cies were collected and identified on cattle. The highest prevalence was observed in Boophilus sp. followed by Hyalomma sp. and Rhipiceph alus sp. (22). We could not detect any Booph- ilus species, but we found R. sanguineus and Hy. anatolicum on cows. These findings are in concordance with the mentioned investi- gation (22). Our investigation shows the presence of 9 species: R. sanguineus (60.05%), R. bursa (0.08), Argas persicus (8.02), Ornithodoros lahorensis (11.83), Hy. marginatum (0.08), Hy. asiaticum (1.49), Hy. anatolicum (12.33), Hy. aegyptium (0.91), Ha. parva (4.22) and Hy- alomma sp. (0.99) in the province. R. san- guineus was the most collected tick sample (726/1209), also, these species were found on all hosts except turtles (Table 1). Rh. sanguineus (brown dog tick) is considered as the most widespread ixodid tick, colonizing both human and animals (31). R. Sanguineus species are very resistant to heat and moisture deficits (32). This species is able to transmit pathogens like Ehrlichia canis to dog (33). They can participate in the epidemiology of canine visceral leishmaniasis (34) and spot- ted fever group rickettsia (35). Some other Ehrlichia associated species in R. sanguineus are E. ewingii, and E. chaffeensis (36). The brown dog tick is also able to trans- mit Rickettsia ricksettsii, causing Rocky Moun- tain Spotted Fever (37), Rickettsia conorii, which is the bacteria responsible for causing Mediterranean spotted fever as well as Rick- ettsia massiliae (38) and R. massiliae (39). Rhipicephalus sanguineus is also reported to transmit Hepatozoon canis (40) as well as Babesiacanis (41). Conclusion Ticks contamination has been detected in a variety of livestock in the Kurdistan region, also the variety of ticks is abundant. The Or- nithodoros and Hyalomma are more important than carriers of known diseases in the Kurdi- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 252–261 O Banafshi et al.: Tick Ectoparasites of … 259 http://jad.tums.ac.ir Published Online: September 30, 2018 stan, including Crimean Congo hemorrhagic fever (CCHF) and tick-borne relapsing fever (TBRF). Regarding the high contamination of live- stock, the presence of disease and borderline province, the importance of the vector con- trol in Kurdistan is more evident, as well as the necessity of further research, especially on the movement of livestock and ticks, as well as the resistance of ticks to the pesticide. 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