http://orcid.org/0000-0003-1614-0756
Figures
Abstract
The importance of tick-borne diseases is increasing all over the world, including Turkey. Global warming, environmental and ecological changes and the existence of suitable habitats increase the impact of ticks and result in frequent emergence or re-emergence of tick-borne diseases (TBDs) with zoonotic characteristics. In Turkey, almost 19 TBDs have been reported in animals and men, involving four protozoa (babesiosis, theileriosis, cytauxzoonosis, hepatozoonosis), one filarial nematode (acanthocheilonemasis), ten bacterial agents (anaplasmosis, ehrlichiosis, aegyptianellosis, tick-borne typhus, Candidatus Rickettsia vini, Lyme borreliosis, tick-borne relapsing fever [TBRF], tularaemia, bartonellosis, and hemoplasmosis), and four viral infections (tick-borne encephalitis [TBE], Crimean-Congo Haemorrhagic Fever [CCHF], louping-ill [LI], and lumpy skin disease [LSD]). The growing number of TBD cases, in particular the fatal viral epidemics in humans, have led to increased public awareness and concern against TBDs in recent years. The World Health Organization (WHO) has developed a new political concept, called the “One Health” initiative, which is especially relevant for developing strategies against tick infestations and TBD control in humans and animals. It would be beneficial for Turkey to adopt this new strategy and establish specific research and control programs in coordination with international organizations like WHO, the World Organization for Animal Health (OIE), the Food and Agriculture Organization (FAO), the Centers for Disease Control and Prevention (CDC), and the European Center for Disease Prevention and Control (ECDC) to combat TBDs based on the “One Health Initiative” concept. In this article, we review the occurrence of primary TBDs in man and animals in Turkey in light of the “One Health” perspective.
Citation: Inci A, Yildirim A, Duzlu O, Doganay M, Aksoy S (2016) Tick-Borne Diseases in Turkey: A Review Based on One Health Perspective. PLoS Negl Trop Dis 10(12): e0005021. https://doi.org/10.1371/journal.pntd.0005021
Editor: Joseph M. Vinetz, University of California San Diego School of Medicine, UNITED STATES
Published: December 15, 2016
Copyright: © 2016 Inci et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Turkey is subtropically located in Eurasia and has a population of over 80 million people, with 50 million livestock animals. The economic structure of Turkey currently depends on a mix of industrial and agricultural products. Turkey is divided into seven distinct geographic regions: Eastern Anatolia, Southeastern Anatolia, Mediterranean, Aegean, Marmara, Black Sea, and Central Anatolia (Fig 1).
The location of Turkey spanning the continents of Europe and Asia is shown. The seven geographic districts with varying ecological characteristics are included on the map. Image credit: The Emirr, Wikipedia Commons.
The geographic location of Turkey provides a natural bridge for transmission of many emerging or re-emerging diseases among the continents of Europe, Asia, and Africa. Particularly, the many marshes or immigrate bird stations (Fig 2), like “Sultan Marshes” in the Kayseri area of Central Anatolia, “Manyas Bird Paradise” in the Marmara region, “Kizilirmak Delta” or “Cernek Ringing Station” in Bafra near Samsun in the Black Sea region, “Hevsel Bird Paradise” in Diyarbakir in the Southeast, and “Aras Bird Paradise” in the Northeast all have high epidemiological importance for the distribution of ticks and tick-borne diseases (TBDs). In addition, the geographic location of Turkey results in highly varied climatic conditions in the seven regions of the country. A typical continental climate prevails in the plateaus of Anatolia, while temperate climates mainly dominate the coastal areas. Each one of the seven geographic regions has different climatic conditions, vegetation structures, and wildlife allowing suitable habitats for various vector arthropods throughout the four seasons of the year.
Image credit: Shadowxfox, Wikipedia Commons.
Many disease pathogens that challenge the welfare of human, livestock, wildlife, and plants worldwide are transmitted to their hosts via specific arthropod vectors [1]. The public health impact and financial consequences of these diseases can devastate the already overburdened economic conditions in developing countries [2], as well as in Turkey [3]. Among these diseases, tick-borne pathogens are the most prevalent and dangerous for public health and livestock, especially during the tick seasons in most parts of Turkey. The morbidity and mortality of TBDs, such as babesiosis, theileriosis, and anaplasmosis annually changes depending on the enzootic stability of infections, and also on the immunological status of host animals. Some TBDs, particularly babesiosis and theileriosis, are known to be prevalent in many parts of Turkey. Tropical theileriosis is widespread in Turkey, with over 90% of animals being seropositive in some areas. Approximately 20%–60% of cattle may be exposed to the disease in one season. Several vector Hyalomma spp. are present in Turkey, and over 40% of ticks can be infected with Theileria annulata in the Central Anatolia, Aegean, and Eastern Anatolia regions. The mortality of infection in local cattle breeds is approximately 50%, but can be up to 100% in imported pure breeds [4]. Meanwhile, a re-emerging disease, Crimean-Congo Haemorrhagic Fever (CCHF), has been associated with many deaths since 2002 and reached a peak in 2008 and 2009, resulting in a total of 126 human deaths in endemic areas of Turkey [5].
In this article, we review the occurrence of TBDs in man and animals in Turkey based on the “One Health” concept. The “One Health” concept was developed to promote interdisciplinary collaborations and communications in all aspects of health care for humans, animals, and the environment. It is expected that this synergism will advance health care by accelerating biomedical research discoveries, enhancing public health efficacy, expanding the scientific knowledge base, and improving medical education and clinical care. Since TBDs equally impact animal and human health, the “One Health” approach is particularly relevant for control of these diseases.
TBDs of Humans and Animals in Turkey
TBDs are caused by several pathogenic agents with global distribution. The pathogens mainly cause destruction of blood cells resulting in anemia, jaundice, hemoglobinuria, anorexia, and weight loss and also increase risk for other bacterial and fungal infections. In Turkey, the ticks that transmit disease belong to both the soft-tick family, Argasidae (genera Argas, Ornithodorus), as well as the hard-tick family, Ixodidae (genera Dermacentor, Hyalomma, Haemaphysalis, Ixodes, and Rhipicephalus) [6–8].
Reported major TBDs include protozoa (babesiosis, theileriosis, cytauxzoonosis, and hepatozoonosis), filarial nematode (acanthocheilonemiasis), rickettsial bacteria (anaplasmosis, ehrlichiosis, aegyptianellosis, tick-borne typhus or Mediterranean spotted fever [MSF], and Candidatus R. vini) and nonrickettsial bacteria (Lyme borreliosis, tick-borne relapsing fever [TBRF], tularemia, bartonellosis, and hemoplasmosis) and viruses (CCHF, tick-borne encephalitis [TBE], louping-ill [LI], and lumpy skin disease [LSD]) (Table 1).
Babesiosis is a zoonotic and hemolytic infection of animals and man caused by Babesia spp., and transovarially and trans-stadially transmitted by ixodid ticks [41]. The disease is characterized by high temperature, anemia, icterus, hemoglobinuria, listlessness, anorexia, and death. Although the major economic impact of babesiosis is on the cattle industry, the infection has been seen in other domestic animals, including horses, sheep, goats, pigs, and dogs, in varying degrees of importance throughout the world [42]. Babesiosis is the first described tick-borne infection in Turkey and has been reported from cattle, sheep/goats, horses, dogs, and man. Bovine and ovine babesiosis are highly prevalent throughout the country, whereas there are no reports about clinical cases of human babesiosis [1,4].
Theileriosis is another tick-borne protozoan disease of ruminants, equids, and felids. The causative agents of the infection belonging to Theileria are transmitted from an infected animal to others by trans-stadial transmission via ticks [43]. The infection appears in two clinical forms in infected animals: malignant and benign theileriosis. The malignant form causes a lymph proliferative disease with high morbidity and mortality in susceptible European cattle breeds, whereas mild infections occur in the indigenous breeds. The main characteristics of the diseases are lymphoid transformation, proliferations, immortalization, and metastasis of schizont-infected monocytes and lymphocytes, resembling cancer [44]. Considerable economic losses have been reported due to malignant cattle theileriosis in endemic areas of the world [45]. Bovine theileriosis is also an important parasitic disease of Turkey. The prevalence of T. annulata infection, morbidity, and mortality was significantly higher in unvaccinated than in vaccinated cattle, whereas the seropositivity was significantly lower in the unvaccinated group. Acute tropical theileriosis cases were diagnosed in 156 of 554 (27.61%) cattle, and 86 of 156 (56.21%) died from the disease in the Cappadocia area of Central Anatolia in Turkey. The total economic losses due to tropical theileriosis were estimated at US$598,133 during 1999–2001 in the area [3]. In addition, ovine theileriosis [1] and equine theileriosis [11] have also been recently reported. Although human theileriosis has not been reported from Turkey, the responsible TBP, T. microti, was shown to circulate in Anatolian squirrel (Spermophilus xanthophrymnus) populations [46].
Cytauxzoonosis is a TBD of domestic cats [47]. The causative agent of the infection, C. felis is transmitted by Amblyomma americanum [48]. Most recently, C. felis was first reported from domestic Van cats in Turkey [12].
Hepatozoonosis is one of the TBDs of dogs. Old World canine hepatozoonosis caused by Hep. canis is transmitted by Rhi. sanguineus, whereas American canine hepatozoonosis caused by Hep. americanum is transmitted by Am. maculatum [49]. In Turkey, Hep. canis infection was detected in dogs [13,50], and mature and immature oocytes as well as sporocysts of Hep. canis were identified in Rhi. sanguineus ticks removed from dogs [9,14].
Anaplasmosis is an opportunistic and widespread vector-borne infection of humans and animals, caused by Anaplasma species including A. marginale, A. centrale, A. bovis, A. ovis for ruminants, A. platys for canines, and A. pagacytophilum for human and domestic animals such as horses. The infection is transmitted mainly intrastadially but also iatrogenically by ticks. The disease is called “Human Granulocytic Anaplasmosis” or “Human Granulocytic Ehrlichiosis” (HGE) in man, “bovine anaplasmosis” in cattle, “ovine anaplasmosis” in sheep, and “canine anaplasmosis” in dogs. The etiologic agent of HGE, A. phagacytophilum, is transmitted intrastadially by Am. americanum ticks in endemic areas [51]. A. phagocytophilum was determined in farm animals [52] and also in humans [53] in Turkey. Additionally, A. phagocytophilum was detected in I. ricinus ticks removed from humans [17]. A few bovine anaplasmosis outbreaks were reported in cattle from some areas [18,54,55], and one A. platys infection was shown in a dog in Turkey [56].
Ehrlichiosis is caused by A. phagocytophilum, E. chaffeesis, and E. ewingii in humans, and called “Human Monocytotropic Ehrlichiosis(HME); A. phagocytophilum and E. canis in dogs, and called “Canine Monocytotropic Ehrlichiosis (CME). The diseases are transmitted by ixodid ticks, and the public health and veterinary importance of Ehrlichiae was emphasized [57]. In Turkey, unfortunately the studies on CME are very limited. However, a few reports have documented seropositivity [19], clinical cases, treatment [20], and molecular prevalence [21,22] of CME in Turkey.
Aegyptianellosis is an intraerythrocytic tick-borne rickettsial infection of amphibians, reptiles, and birds. The infection is caused by Ae. pullorum and is transmitted to fowls by Argas persicus ticks [58,59]. One Ae. pullorum infection case was reported from ducks in Turkey [23].
Tick-borne Typhus is one of the oldest tick-borne rickettsial diseases. In Turkey, several cases of MSF associated with R. conorii have been reported from humans [60–64]. Recently, R. hoogstraali and two human pathogenic species (R. aeschlimannii and R. slovaca) were detected in ixodid ticks in Turkey [10,24]. Candidatus R. vini was detected in I. arboricola ticks collected from birds in the Kizilirmak Delta of Turkey [8].
Lyme borreliosis is a widespread and zoonotic tick-borne bacterial infection of humans and dogs in the north hemisphere [65]. Lyme disease is caused by spirochetes that comprise a complex referred to as Bor. burgdorferi sensu lato, with five major species that cause human disease. Bor. burgdorferi is used to refer to the whole complex and transmitted to humans and dogs by Ixodes spp. [66]. In Turkey, Bor. burgdorferi was isolated from I. ricinus ticks collected from cattle in the Black Sea region in 1998 [25], and spirochetes of Borrelia were present in an unfed tick nymph [67]. Meanwhile, some Bor. burgdorferi sensu lato strains were characterized molecularly [26], and a novel Borrelia sp. was also isolated from H. aegyptium ticks collected from tortoises (Testudo graeca) [27], and the spirochete was named as Bor. turcica sp. nov. [28]. A clinical Lyme case was observed in a dog in 2007 [68], and anti-Bor. burgdorferi antibodies were detected in dogs and horses in Turkey [69]. Recently, Bor. burgdorferi sensu stricto was isolated from unusual tick species, H. marginatum, H. excavatum, Hae. parva, and nymphs of Hyalomma spp. in Turkey [24].
TBRF is a spirochete disease of man caused by Borrelia spp. associated with the bite or coxal fluid of argasid ticks of the genus Ornithodoros in a wider endemic geographic area of the world and occurs in Africa, Asia, and the Americas with different Borrelia tick vector complexes in each area [66]. In Turkey, the presence of relapsing fever with a spirochete of the Crocidurae group, Bor. crocidurae, was also shown in O. erraticus ticks collected from rodent holes in the southeastern areas near the Syria border [29].
Tularemia is an arthropod-transmitted zoonotic bacterial infection caused by the F. tularensis and comprises a range of clinical syndromes ranging from mild to very severe. The majority of cases occur in the northern hemisphere, particularly in rural or semirural environments [66]. In Turkey, tularemia is an important disease, which has re-emerged in 1988, and the first tularemia outbreak was recorded in 2005 [70]. The first case associated with the outbreak was diagnosed near Kayseri, and the region was described as an endemic area for tularemia [30], but no positivity was detected in pools of mosquitoes and ticks collected near the Kayseri area by molecular techniques [31].
Bartonellosis is another zoonotic vector-borne infection of humans that is caused by Bar. henselae, with a large distribution in the northern hemisphere [71]. Domestic cats represent the main reservoir of the pathogen, and the main vector of the infection is the cat flea [72]. However, the trans-stadial transmission of Bar. henselae by I. ricinus ticks was also shown [73]. In Turkey, a solitary study on bartonellosis was reported in domestic cats [32].
Hemoplasmosis is one of the bacterial infections of humans and animals caused by Mycoplasma spp. [74]. Although the infection is mainly described as vector-borne and transmitted by blood-feeding arthropods such as ticks and fleas, the disease might also be transmitted through other routes, such as mechanically with contaminated operation tools or blood transfusions and vertically in the intra-uterine period [75]. Rhi. appendiculatus transmits the infection to dogs by cofeeding [76]. In Turkey, a clinical case about feline hemoplasmosis-associated M. haemofelis was reported [33].
TBE is an important infection of humans prevalent in a large endemic area of Asia and Europe. The disease agent is a virus belonging to the genus Flavivirus [77]. In Turkey, a few serosurveys were performed in the Southeast [34], the Central Anatolia [35] and Aegean regions [36,37], and in Central/Northern Anatolia [78], in which the seropositivities were reported in the range of 1.4% to 20.5%.
CCHF is a contagious and re-emerging infection of man transmitted by several ixodid ticks [79]. Wild and livestock animals serve as amplifiers of the CCHF virus in field conditions [38]. In Turkey, the infection was first observed in 2002 around Tokat in the Black Sea region and spread to neighboring cities initially and then throughout the country [80,81]. There has been an increase in the cases in following years, reaching a peak in 2008 and 2009, with a decrease thereafter. However, nearly 900 new CCHF cases are now seen annually, and a total of 9,787 cases have been reported from 2002 through 2015, resulting in 469 deaths (4.79%) [5].
LI is a tick-transmitted and acute viral disease of mainly sheep/goats, but it can sometimes also affect cattle and horses. The LI virus characteristically causes an encephalomyelitis disease of sheep. The occurrence of LI was found closely related to the distribution of the primary vector tick, I. ricinus, and the infection was reported from various countries including England, Norway, Greece, and Bulgaria [82], as well as the northwestern part of Turkey [39].
LSD is a pox disease of cattle characterized with nodules on the skin, transmitted mechanically via blood-feeding arthropods, including some hard ticks. It was reported that Rhi. (Boophilus) decoloratus, Rhi. appendiculatus, and Am. hebraeum ticks have a transmission role in the epidemiology of LSD in the endemic areas [83]. An LSD outbreak was recognized in cattle associated with the nodular clinical symptoms in Turkey [40]. Recently, a new confirmed LSD outbreak with huge economical devastation has been reported by official government veterinaries in May and June months of 2016 in Aegean region of Turkey and more than 500 cattle infected with LSD virus have been culled for the control of the disease (Prof. Abdullah Inci, personal communication).
Conclusion
In this review, we focused on the assessment of TBDs in Turkey with a holistic approach. Turkey’s natural conditions allow exposure to many tick-borne infections in animals and humans in different regions. A total of 19 tick-borne infections have already been reported from seven major regions of Turkey. Many of these diseases result in significant economic losses and pose major public health threats. Millions of migratory birds, which utilize the sanctuaries present in Turkey during their annual migration, pose a constant threat to the spread of new infectious agents. Despite the high endemicity of tick borne pathogens and presence of suitable tick habitats in Turkey, in depth epidemiological studies and research investigations into TBDs are lacking. Thus, Turkey urgently needs to develop a new disease management strategy and establish the infrastructure for control programs against ticks and TBDs. We propose that a new framework be adopted in coordination with international bodies including WHO, the World Organization for Animal Health (OIE), the Food and Agriculture Organization (FAO), the Centers for Disease Control and Prevention (CDC), and the European Center for Disease Prevention and Control (ECDC) based on the modern concept “One Health Initiative” or “One Medicine Perspective.” This strategy should include predictable scenarios for the future of TBDs based on knowledge of the host—pathogen—tick “disease triangle” with regards to global warming, environmental changes, and socioeconomic status of affected human societies and the ecology of tick habitats and tick distributions. To interfere with this triangle, the first and urgent step is to organize and initiate an integrated tick control program through the disease endemic regions of the country. Towards this purpose, the application of new and advanced tick control techniques, such as recombinant anti-tick vaccines applicable for animals, can be investigated. Support of crosscutting and interdisciplinary tick research projects in specialized research centers would facilitate knowledge and future applications. Another important approach is to improve disease-resistant animals instead of susceptible breeds against TBDs using vaccination and immunization programs, especially for babesiosis, theileriosis, and anaplasmosis. At this point, the development of the CCHF vaccine is of critical importance in order to control disease in the human host in endemic areas of Turkey.
In accordance with the “One Health” concept, development of advanced research projects for control of ticks and TBDs by expert researchers from all related scientific disciplines should be a top priority. On the other hand, the administrative and political decisions that impact climate change, urbanization, land use, and industrial and agricultural pollution should be consistent with ecological and epidemiological findings on ticks and TBDs in Turkey. We also suggest that a regional program utilizing the One Health Concept that takes into account an interdisciplinary approach would be imperative to combat TBDs given that country borders are insignificant for disease transmission. Turkey should provide leadership to bring together the agencies and appropriate researchers under the auspices of international organizations to help shape a global policy for TBD control in the region.
Top Five Papers
- Inci A, Yazar S, Tuncbilek AS, Canhilal R, Doganay M, Aydin L, et al. Vectors and vector-borne Diseases in Turkey. Ankara Univ Vet Fak Derg. 2013; 60: 281–96.
- Sayin F, Dincer D, Karaer Z, Cakmak A, Inci, A, Yukari BA, et al. Tick-borne diseases in Turkey. Trop Anim Hlth Prod. 1997; 29: 535.
- Aydin L, Bakirci S. Geographical distribution of ticks in Turkey. Parasitol Res. 2007; 101(Suppl 2): S163-6.
- Leblebicioglu H, Ozaras R, Irmak H, Sencan I. Crimean-Congo hemorrhagic fever in Turkey: Current status and future challenges. Antiviral Res. 2016;126: 21–34.
- Inci A, Ica A, Yildirim A, Vatansever Z, Cakmak A, Albasan H, et al. Economical impact of tropical theileriosis in the Cappadocia region of Turkey. Parasitol Res. 2007;101 (Suppl 2): S171-4.
Key Learning Points
- The geographic location of Turkey serves as a natural bridge for transmission of many emerging or re-emerging diseases among the continents of Europe, Asia, and Africa.
- Several argasid (genera Argas, Ornithodorus) and ixodid tick species (genera Dermacenter, Hyalomma, Haemaphysalis, Ixodes, and Rhipicephalus) have been responsable for the transmission of TBPs.
- Until today, 19 TBDs have already been reported in Turkey with a high economical impact.
- New disease management strategies and control programs against ticks and tick-borne infections should be put into practice based on the “One Health” concept in Turkey.
References
- 1. Inci A, Yazar S, Tuncbilek AS, Canhilal R, Doganay M, Aydin L, et al. Vectors and vector-borne Diseases in Turkey. Ankara Univ Vet Fak Derg. 2013; 60: 281–96.
- 2.
Aksoy S. Transgenesis and the management of vector-borne disease. In: Aksoy S, editor. Advances in Experimental Medicine and Biology. Springer Science + Business Media, LLC, Landens Bioscience, Vol 627; 2008.
- 3. Inci A, Ica A, Yildirim A, Vatansever Z, Cakmak A, Albasan H, et al. Economical impact of tropical theileriosis in the Cappadocia region of Turkey. Parasitol Res. 2007; 101 (Suppl 2): S171–4.
- 4. Sayin F, Dincer D, Karaer Z, Cakmak A, Inci A, Yukari BA, et al. Tick-borne diseases in Turkey. Trop Anim Hlth Prod. 1997; 29: 535.
- 5. Leblebicioglu H, Ozaras R, Irmak H, Sencan I. Crimean-Congo hemorrhagic fever in Turkey: Current status and future challenges. Antiviral Res. 2016; 126: 21–34. pmid:26695860
- 6. Aydin L, Bakirci S. Geographical distribution of ticks in Turkey. Parasitol Res. 2007; 101(Suppl 2): S163–6.
- 7. Bursali A, Keskin A, Tekin S. A review of the ticks (Acari:Ixodida) of Turkey: species diversity, hosts and geographical distribution. Exp Appl Acarol. 2012; 57:91–104. pmid:22371208
- 8. Keskin A, Koprulu TK, Bursali A, Ozsemir AC, Yavuz KE, Tekin S. First record of Ixodes arboricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). J Med Entomol. 2014; 51(4): 864–7. pmid:25118420
- 9. Aktas M. A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol. 2014; 200: 276–83. pmid:24424312
- 10. Orkun O, Karaer Z, Cakmak A, Nalbantoglu S. Identification of tick-borne pathogens in ticks feeding on humans in Turkey. Plos NTD. 2014; 8(8): e3067.
- 11. Kizilaslan F, Yildirim A, Duzlu O, Inci A, Onder Z, Ciloglu A. Molecular detection and characterization of Theileria equi and Babesia caballi in horses (Equus ferus caballus) in Turkey. J Equine Vet Sci. 2015; 35: 830–5.
- 12. Karaca M, Akkan HA, Tutuncu M, Ozdal N, Deger S, Agaoglu ZT. Cytauxzoonosis in Van cats. YYU Vet Fak Derg. 2007; 18(1): 37–9.
- 13. Tuzdil AN. Bizde ilk defa gorulen bir Hepatozoon canis vak’asi. Turk Baytarlar Cemiyeti Mecmuasi. 1933; 13: 35(In Turkish).
- 14.
Ozubek S, Sayin Ipek DN, Aktas M. Kenelerde Hepatazoon canis ookistinin mikroskobik gorunumu. 19. Ulusal Parasitoloji Kongresi ve Uluslararasi katilimli Ekinokokosis Sempozyumu, 5–9 Ekim, Erzurum, 2015. p. 194 (In Turkish).
- 15.
Erdil N. Kopeklerde Dirofilaria immitis ve Dipetalonema reconditum uzerinde arastirma. KKK As Vet Akademisi Ic Hastaliklar Sube ve Klinigi Calismalari, Ankara, 1966 (In Turkish).
- 16. Toparlak M, Gargili A, Ulutas Esatgil M, Cetinkaya H. Canine filariosis around Istanbul, Turkey Employing Naphtol AS-TRm phosphate. Acta Vet Brno. 2005; 74: 233–6.
- 17. Aktas M, Vatansever Z, Altay K, Aydin MF, Dumanli N. Molecular evidence for Anaplasma phagocytophilum in Ixodes ricinus from Turkey. Trans R Soc Trop Med Hyg. 2010; 104: 10–5. pmid:19744685
- 18. Aktas M, Altay K, Dumanli N. Molecular detection and identification of Anaplasma and Ehrlichia species in cattle from Turkey. Ticks Tick Borne Dis. 2011; 2: 62–5. pmid:21771539
- 19. Sari B, Tasci GT, Kilic Y. Seroprevalence of Dirofilaria immitis, Ehrlichia canis and Borrelia burgdorferi in dogs in Igdir province, Turkey. Kafkas Univ Vet Fak Derg. 2013; 19 (5): 735–9.
- 20. Aysul N, Ural K, Cetinkaya H, Kuskucu M, Toros G, Eren H, et al. Doxycycline-chloroquine combination for treatment of canine monocytic ehrlichiosis. Acta Sci Vet. 2012; 40: 1031.
- 21. Unver A, Rikihisa Y, Borku K, Ozkanlar Y, Hanedan B. Molecular detection and characterization of Ehrlichia canis from dogs in Turkey. Berl Munch Tierarztl Wochenschr, 2005; 118: 300–4. pmid:16048040
- 22. Duzlu O, Inci A, Yildirim A, Onder Z, Ciloglu A. Kopeklerde kene kaynakli bazi protozoon ve rickettsial enfeksiyonlarin Real Time PCR ile arastirilmasi ve saptanan izolatlarin moleküler karakterizasyonlari. Ankara Univ Vet Fak Derg. 2014; 61: 275–82 (In Turkish).
- 23. Pusat MM. Memleketimizde ilk defa tesbit edilen Aegyptionella pullorum vak’asi. Turk Vet Hek Dern Derg. 1955; 25 (108–109): 2487–90 (In Turkish).
- 24. Orkun O, Karaer Z, Cakmak A, Nalbantoglu S. Spotted fever group rickettsiae in ticks in Turkey. Ticks Tick-borne Dis. 2014; 5: 213–8. pmid:24355764
- 25. Polat E, Calisir B, Yucel A, Tuzer E. Turkiye'de Ixodes ricinus'lardan ilk defa ayrilan ve uretilen iki Borrelia kokeni. Turkiye Parazitol Derg. 1998; 22: 167–73 (In Turkish).
- 26. Guner ES, Hashimoto N, Takada N, Kaneda K, Imai Y, Masuzawa T. First isolation and characterization of Borrelia burgdorferi sensu lato strains from Ixodes ricinus ticks in Turkey. J Med Microbiol. 2003; 52: 807–13. pmid:12909659
- 27. Guner ES, Hashimoto N, Kadosaka T, Imai Y, Masuzawa T. A novel, fast growing Borrelia sp. isolated from the hard tick Hyalomma aegytium in Turkey. Mikrobiol. 2003;149: 2539–44.
- 28. Guner ES, Watanabe M, Hashimoto N, Kadosaka T, Kawamura Y, Ezaki T, et al. Borrelia turcica sp. nov., isolated from the hard tick Hyalomma aegyptium in Turkey. Int J Syst Eval Microbiol. 2004; 54:1649–52.
- 29. Ozsan K, Akyay N. Relapsing fever in Turkey; presence in the South (Turko-Syrian border) of Ornithodorus erraticus infected with a spirochete of the Crocidurae group. Bull Soc Pathol Exot Filiales. 1954;47: 501–3. pmid:13230802
- 30. Ulu-Kilic A, Doganay M. An overview: Tularemia and travel medicine. Travel Med Infect Dis. 2014; 12: 609–16. pmid:25457302
- 31. Duzlu O, Yildirim A, Inci A, Gumussoy SK, Ciloglu A, Onder Z. Molecular investigation of Francisella-like endosymbiont in ticks and Francisella tularensis in ixodid ticks and mosquitoes in Turkey. Vector Borne Zoonotic Dis. 2016; 16(1): 26–32. pmid:26741324
- 32. Celebi B, Kilic S, Aydin N, Tarhan G, Carhan A, Babur C. Investigation of Bartonella henselae in cats in Ankara, Turkey. Zoonoses Public Health. 2009; 56: 169–75. pmid:18990198
- 33. Tuzer E, Goksu K, Bilal T, Yesildere T. A case of haemobartonellosis in a cat in Istanbul. J Protozool Res. 1993; 3: 69–70.
- 34. Ergunay K, Ozer N, Us D, Ozkul A, Simsek F, Kaynas S. Seroprevalence of West Nile virus and tick-borne encephalitis virus in southeastern Turkey: first evidence for tick-borne encephalitis virus infections. Vector Borne Zoonotic Dis. 2007; 7: 157–61. pmid:17627432
- 35. Uyar Y, Akcali A, Carhan A, Ozkaya E, Ertek M. Seroprevalence of tick-borne encephalitis virus (TBEV) among cases with tick bite history in Turkey. Turk Hij Deney Biyol Derg. 2007; 64: 21–5.
- 36. Serter F. Tick-borne meningo-encephalitis cases in Izmir area. EU Tip Fak Mecmuasi. 1968; 7:1–13.
- 37. Esen B, Gozalan A, Coplu N, Tapar FS, Uzan R, Aslan T, et al. The presence of tick-borne encephalitis in an endemic area for tick-borne diseases, Turkey. Trop Doct. 2008; 38: 27–8. pmid:18302859
- 38.
Vatansever Z, Uzun R, Estrada-Pena A, Ergonul O. Crimean-Congo hemorrhagic fever in Turkey. In: Ergonul O, Whitehouse CA, editors. Crimean-Congo hemorrhagic fever: a global perspective. Dordrecht, Springer; 2007.
- 39. Hardly WJ, Martin WB, Hakioğlu F, Chifney STE. A viral encephalitis of sheep in Turkey. Pendik Institute J. 1969;1:89–100.
- 40. Inci A, Yildirim A, Duzlu O. Three emerging vector-borne diseases in Turkey. Erciyes Univ Vet Fak Derg. 2014; 11(2): 117–20.
- 41. Uilenberg G. Babesia- a historical overview. Vet Parasitol. 2006; 138: 3–10. pmid:16513280
- 42.
Estrada-Pena A, Farkas R, Jaenson TGT, Koenen F, Madder M, Pascucci I, et al. Ticks and Tick-Borne Diseases geographical distribution and control strategies in the Euro-Asia region. Salman M, Tarres-Call J (eds), CAB International, UK, 2013. p.292.
- 43. Robinson PM. Theileria annulata and its transmission-A review. Trop Anim Health Prod. 1982; 14: 3–12. pmid:6805112
- 44.
Dobbelaere D, McKeever D. Introduction. In: Dobbelaere D, McKeever D, Black SJ, Seed JR, editors. World Class Parasites: Volume 3 Theileria. Kluwer Academic Publishers; 2002. pp. IX–X.
- 45. Gharbi M, Sassi L, Dorchies P, Darghouth MA. Infection of calves with Theileria annulata in Tunisia: economic analysis and evaluation of the potential benefit of vaccination. Vet Parasitol. 2006; 137: 231–41. pmid:16481113
- 46. Cicek H, Karatepe M, Cakir M, Eser M. Nigde yoresinde Anadolu tarla sincabi, Spermophilus xanthophrymnus (Rodentia: Sciuridae)’da bulunan kan parazitleri. Ankara Univ Vet Fak Derg. 2009; 56: 147–8 (In Turkish).
- 47. Cohn LA. Feline Cytauxzoonosis. AAFP Rounds. 2005; 27: 69–75.
- 48. Reichard MV, Meinkoth JH, Edwards AC, Snider TA, Kocan KM, Blouin EF, et al. Transmission of Cytauxzoon felis to a domestic cat by Amblyomma americanum. Vet Parasitol. 2009;161(1–2): 110–5. pmid:19168288
- 49.
Baneth G. Hepatozoonosis canine. In: Service NW, editor. The Encyclopedia of arthropod-transmitted infections of man and domesticated animals. CABI Publishing, NY; 2006. p. 215–220.
- 50. Karagenc TI, Pasa S, Kirli G, Hosgor M, Bilgic HB, Ozon YH, et al. A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Vet Parasitol. 2006; 135: 113–9. pmid:16229952
- 51. Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol. 2010;167: 95–107. pmid:19811876
- 52. Gokce HI, Genc O, Akca A, Vatansever Z, Unver A, Erdogan HM. Molecular and serological evidence of Anaplasma phagocytophilum infection of farm animals in the Black sea region of Turkey. Acta Vet Hung. 2008; 56(3): 281–92. pmid:18828480
- 53. Gunes T, Poyraz O, Atas M, Turgut NH. The seroprevalence of Anaplasma phagocytophilum in humans from two different climatic regions of Turkey and its co-seroprevalence rate with Borrelia burgdorferi. Turk J Med Sci. 2011; 41: 903–8.
- 54. Ozlem MB, Karaer Z, Turgut K, Eren H, Irmak K, Inci A. Efficacy of long-acting oxytetracycline on bovine anaplasmosis. Ank Univ Vet Fak Derg. 1988; 35:1–5.
- 55. Birdane FM, Sevinc F, Derinbay O. Anaplasma marginale infections in dairy cattle: clinical disease with high seroprevalence. Bull Vet Inst Pulawy. 2006; 50: 467–70.
- 56. Ulutas B, Bayramli G, Karagenc T. First case of Anaplasma (Ehrlichia) platys infection in a dog in Turkey. Turk J Vet Animal Sci. 2007; 31: 279–82.
- 57.
Gaff HD, Kocan KM, Sonenshine DE. Tick-borne rickettsioses II (Anaplasmataceae). In: Sonenshine DE, Roe RM, editors. Biology of Ticks. Vol 2, Second edt, Oxford University, Oxford, New York; 2014. p. 251–77.
- 58. Bedford GAH, Coles JDWA. The transmission of Aegyptianella pullorum, Carpano, to fowls by means of ticks belonging to the genus Argas. Onderstepoort J Vet Sci Anim Ind. 1933.1.
- 59. Castlle MD, Christensen BM. Isolation and identification of Aegyptianella pullorum (Ricketsttiales, Anaplasmataceae) in wild turkeys from North America. Avian Dis. 1985; 29(2): 437–45. pmid:4026738
- 60.
Seber E, Yaflar AY, Cetin BD, Sucu R. Riketsiyoz: bes vaka. VI. Turk Klinik Mikrobiyoloji ve Infeksiyon Hastaliklari Kongresi, 15–17 Eylul, Trabzon. 1992. p. 44 (In Turkish).
- 61. Mert A, Tabak F, Dumankar A, Eroglu C, Ozturk R, Aktuglu Y. Dort Marsilya humması vakasi. Klimik Derg. 1997; 10(3): 146–8 (In Turkish).
- 62. Coskun D, Ozyurek S, Goktas P. Bir Akdeniz benekli ates vakasi. Flora. 1999; 4:72 (In Turkish).
- 63. Erten N, Karan MA, Tascioglu C, Yurci A, Dilmener M, Kaysi A. Rickettsia conorii infeksiyonu: vaka sunusu. Klimik Derg. 2000; 13(1): 36–8 (In Turkish).
- 64. Ozgunes N, Ergen P, Yazici S, Aksoy Y, Bekler G, Sargin F. Yirmi riketsiyoz vakasi. Klimik Derg. 2001; 14(2): 91–2 (In Turkish).
- 65.
Kurtenbach K. Lyme borreliosis. In: Service MW, editor. The Encyclopedia of Arthropod-transmitted Infections of Man and Animals. CABI Publishing, UK; 2006. p. 299–305.
- 66.
Ogden NH, Artsob H, Margos G, Tsao J. Non-rickettsial tick-borne bacteria and the diseases they cause. In: Sonenshine DE, Roe RM, editors. Biology of Ticks. Vol 2, Second edt, Oxford University Press, Oxford, New York; 2014. p. 278–312.
- 67. Calisir B, Polat E, Guney G, Gonec L. Investigation on the species composition of the Ixodid ticks from Belgrade forest in Istanbul and their role as vectors of Borrelia burgdorferi. Acta Zool Bulg. 2000; 52: 23–8.
- 68. Gulanber EG, Gulanber A, Albayrak R. 2007. Lyme disease (borreliosis) in a Saint Bernard dog: First clinical case in Turkey. Turk J Vet Anim Sci. 31(5): 367–9.
- 69. Bhide M, Yilmaz Z, Golcu Z, Torun S, Mikula I. Seroprevalence of anti-Borrelia burgdorferi antibodies in dogs and horses in Turkey. Ann Agric Environ Med. 2008; 15: 85–90. pmid:18581984
- 70. Kilic S. Francisella tularensis ve Turkiye’de tularemi epidemiyolojisine genel bir bakis. Flora. 2010;15:37–58 (In Turkish).
- 71. Chomel BB, Kasten RW. Bartonellosis, an increasingly recognized zoonosis. J Appl Microbiol. 2010; 109(3): 743–50. pmid:20148999
- 72.
Chomel BB, Chang C. Cat-scratch and other related Bartonella infections. In: Service MW, editor. The Encyclopedia of Arthropod-transmitted Infections of Man and Domesticated Animals. CABI Publishing, UK; 2006. p.107–10.
- 73. Cotté V, Bonnet S, Le Rhun D, Le Naour E, Chauvin A, Boulouis HJ, et al. Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis. 2008; 14(7): 1074–80. pmid:18598628
- 74. Willi B, Boretti FS, Tasker S, Meli ML, Wengi N, Reusch CE, et al. From Haemobartonella to hemoplasma: molecular methods provide new insights. Vet Microbiol. 2007;125: 197–209. pmid:17706380
- 75. Messick JB. Hemotrophic mycoplasmas (hemoplasmas): a review and new insights into pathogenic potential. Vet Clin Pathol. 2004; 33: 2–13. pmid:15048620
- 76. Maggi RG, Compton SM, Trull CL, Mascarelli PE, Mozayeni BR, Breitschwerdt EB. Infection with hemotropic Mycoplasma species in patients with or without extensive arthropod or animal contact. J Clin Microbiol. 2013; 51(10): 3237–41. pmid:23863574
- 77.
Heinz FX, Holzmann H. Tick-borne encephalitis. In: Servic MW, editor. The Encyclopedia of Arthropod-transmitted Infections. CABI Publishing, UK; 2006. p. 507–12.
- 78. Ergunay K, Saygan MB, Aydogan S, Litzba N, Sener B, Lederer S, et al. Confirmed exposure to tick-borne encephalitis virus and probable human cases of tick-borne encephalitis in Central/Northern Anatolia, Turkey. Zooneses Public Health. 2011; 58: 220–7.
- 79.
Nuttall PA. Tick-borne viruses. In: Soneneshine DE, Roe RM, editors. Biology of ticks. Vol 2, Second edt, Oxford University Press, Oxford, New York; 2014. p. 180–210.
- 80. Ergonul O. Crimean-Congo hemorrhagic fever. Lancet Infect Dis. 2006; 6: 203–14. pmid:16554245
- 81. Gunes T, Poyraz O, Vatansever Z. Crimean-Congo hemorrhagic fever virus in ticks collected from humans, livestock, and picnic sites in the hyper endemic region of Turkey. Vector Borne Zoonotic Dis. 2011;11: 1411–6. pmid:21736490
- 82.
Gould EA. Louping ill, sheep. In: Service MW, editor. The Encyclopedia of Arthropod-transmitted Infections of Man and Domesticated Animals. CABI Publishing, UK; 2006. p. 290–4.
- 83. Tuppurainen ESM, Stoltsz WH, Troskie M, Wallace DB, Oura CAL, Mellor PS, et al. A potential role for ixodid (hard) tick vectors in the transmission of lumpy skin disease virus in cattle. Transbound Emerg Dis. 2011; 58: 93–104. pmid:21114790