Zoonotic pathogens associated with Hyalomma aegyptium in endangered tortoises: evidence for host-switching behaviour in ticks?

Particle and Fibre Toxicology

Vasile Cozma²  Călin M Gherman²  Menelaos Lefkaditis¹  Attila D Sándor²  Zsuzsa Kalmár²  Mirabela O Dumitrache²  Gianluca D’Amico²  Andrei D Mihalca²  Ioana A Matei²  Anamaria I Paștiu² 

[1] Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Thessaly, Trikalon 224, PO Box 199, Karditsa, 43100, Greece;Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Calea Mănăștur 3-5, Cluj-Napoca, 400372, Romania

关键词: Coxiella burnetii;    Ehrlichia canis;    Anaplasma phagocytophilum;    Borrelia burgdorferi s.l;    Testudo graeca;    Hyalomma aegyptium;   

Others  :  1228104
DOI  :  10.1186/1756-3305-5-301

 received in 2012-11-15, accepted in 2012-12-23,  发布年份 2012

【 摘 要 】

Background

Hyalomma aegyptium is a hard-tick with a typical three-host life cycle. The main hosts are Palearctic tortoises of genus Testudo. However, other hosts can be used by immature ticks for feeding in natural conditions. Given this complex ecology and multiple host use, the circulation of pathogens by H. aegyptium between various hosts can be important from epidemiological point of view. The aim of this study was to evaluate the role of H. aegyptium as natural carrier of four important zoonotic pathogens.

Methods

From 2008 to 2011, 448 H. aegyptium ticks were collected from 45 Spur-thighed tortoises, Testudo graeca in Romania. DNA was extracted individually from each tick using a commercial kit. DNA was examined for the presence of specific sequences of Borrelia burgdorferi s.l., Anaplasma phagocytophilum, Ehrlichia canis and Coxiella burnetii by PCR, according to previously described protocols.

Results

PCR analysis of H. aegyptium revealed the presence of A. phagocytophilum (18.8%), E. canis (14.1%) and C. burnetii (10%). 32.4% of the ticks were infected with at least one pathogen and 9.8% had co-infections. The stages most frequently infected were nymphs (50%) followed by males (33.9%) and females (27%). The number of tortoises which harboured infected ticks was 27/45 examined (60%). From all tested T. graeca, 40% harboured ticks infected with A. phagocytophilum, 46.7% had ticks infected with E. canis and 33.3% had ticks with C. burnetii. This study reports for the first time the presence of A. phagocytophilum and E. canis in H. aegyptium.

Conclusions

The presence and relatively high prevalence of three important zoonotic pathogens in H. aegyptium raises the question of their epidemiologic importance in disease ecology. As tortoises are unlikely to be reservoir hosts for A. phagocytophilum and E. canis and both these pathogens are common in H. aegyptium, this is an important indication for (1) a possible increased host-switching behaviour of these ticks to competent reservoir hosts (i.e. hedgehogs) and (2) transstadial transmission. Furthermore, if we consider also the presence of C. burnetii, we conclude that T. graeca and its ticks should be evaluated more seriously when assessing the eco-epidemiology of zoonotic diseases.

【 授权许可】

   
2012 Paștiu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 1.

【 参考文献 】

• [1]Apanaskevich DA: Host–parasite relationships of the genus Hyalomma Koch (Acari, Ixodidae) and their connection with microevolutionary processes. Parazitologiya 2004, 38:515-523. in Russian
• [2]Mihalca AD, Gherman CM, Cozma V: Coendangered hard-ticks: threatened or threatening? Parasit Vectors 2011, 4:71. BioMed Central Full Text
• [3]Kolonin GV: Mirovoe rasprostranenie iksodovykh kleshchey. Rody Hyalomma, Aponomma, Amblyomma [World distribution of ixodid ticks. Genera Hyalomma, Aponomma, Amblyomma]. Moskva, SSSR: Nauka; 1983. in Russian
• [4]Apanaskevich DA: K diagnostike vida Hyalomma (Hyalomma) aegyptium (Acari, Ixodidae) [To diagnostics of Hyalomma (Hyalomma) aegyptium (Acari: Ixodidae)]. Parazitologiya 2003, 37:47-59. in Russian
• [5]Široký P, Petrželková KJ, Kamler M, Mihalca AD, Modrý D: Hyalomma aegyptium as dominant tick in tortoises of the genus Testudo in Balkan countries, with notes on its host preferences. Exp Appl Acarol 2006, 40:279-290.
• [6]Hoogstraal H: African Ixodoidea. I. Ticks of the Sudan. Washington, DC, USA: Department of the navy, bureau of medicine and surgery; 1956.
• [7]Hoogstraal H, Kaiser MN: Some host relationships of the tortoise tick.Hyalomma (Hyalommasta) aegyptium(L.) (Ixodoidea, Ixodidae) in Turkey. Ann Entomol Soc Am 1960, 53:457-458.
• [8]Kolonin GV: Reptiles as hosts of ticks. Russ J Herp 2004, 11:177-180.
• [9]Vatansever Z, Gargili A, Aysul NS, Sengoz G, Estrada-Peña A: Ticks biting humans in the urban area of Istanbul. Parasitol Res 2008, 102:551-553.
• [10]Bursali A, Tekin S, Orhan M, Keskin A, Ozkan M: Ixodid ticks (Acari: Ixodidae) infesting humans in Tokat Province of Turkey: species diversity and seasonal activity. J Vector Ecol 2010, 35:180-186.
• [11]De Sousa R, Lopes De Carvalho I, Santos AS, Bernardes C, Milhano N, Jesus J, Menezes D, Núncio MS: Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl Environ Microbiol 2012, 78:3767-3769.
• [12]Ray HN: Hereditary transmission of Theileria annulata infection in the tick, Hyalomma aegyptium Neum. Trans R Soc Trop Med Hyg 1950, 44:93-104.
• [13]Güner ES, Watanabe M, Hashimoto N, Kadosaka T, Kawamura Y, Ezaki T, Kawabata H, Imai Y, Kaneda K, Masuzawa T: Borrelia turcica sp. nov., isolated from the hard tick Hyalomma aegyptium in Turkey. Int J Sys Evol Micr 2004, 54:1649-1652.
• [14]Kar S, Yılmazer N, Midilli K, Ergin S, Alp H, Gargılı A: Presence of the zoonotic Borrelia burgdorferi s.l. and Rickettsia spp. in the ticks from wild tortoises and hedgehogs. J Marmara Univ Inst Health Sci 2011, 1:166-170.
• [15]Sergent ED, Sergent ET: Sur une hémogrégarine, parasite de Testudo mauritanica. C R Soc Biol 1904, 56:130-131.
• [16]Paperna I, Kremer-Mecabell T, Finkelman S: Hepatozoon kisrae n. sp. infecting the lizardAgama stelliois transmitted by the tickHyalommacf.aegyptium. Parasite 2002, 9:17-27.
• [17]Bitam I, Kernif T, Harrat Z, Parola P, Raoult D: First detection of Rickettsia aeschlimannii in Hyalomma aegyptium from Algeria. Clin Microbiol Infect 2009, 15:253-254.
• [18]Široký P, Kubelová M, Modrý D, Erhart J, Literák I, Špitalská E, Kocianová E: Tortoise tick Hyalomma aegyptium as long term carrier of Q fever agent Coxiella burnetii - evidence from experimental infection. Parasitol Res 2010, 107:1515-1520.
• [19]Mihalca AD, Dumitrache MO, Magdaş C, Gherman CM, Domşa C, Mircean V, Ghira IV, Pocora V, Ionescu DT, Sikó Barabási S, Cozma V, Sándor AD: Synopsis of the hard ticks (Acari: Ixodidae) of Romania with update on host associations and geographical distribution. Exp Appl Acarol 2012, 58:183-206.
• [20]Yadav MP, Sethi MS: Poikilotherms as reservoirs of Q-fever (Coxiella burnetii) in Uttar Pradesh. J Wildl Dis 1979, 15:15-17.
• [21]Majláthová V, Majláth I, Hromada M, Tryjanowski P, Bona M, Antczak M, Víchová B, Dzimko S, Mihalca A, Pet’ko B: The role of the sand lizard (Lacerta agilis) in the transmission cycle of Borrelia burgdorferi sensu lato. Int J Med Microbiol 2008, 298:161-167.
• [22]Peter TF, Burridge MJ, Mahan SM: Competence of the African tortoise tick, Amblyomma marmoreum (Acari: Ixodidae), as a vector of the agent of heartwater (Cowdria ruminantium). J Parasitol 2000, 86:438-441.
• [23]Široký P, Kamler M, Modry D: Long-term occurrence of Hemoliviacf.mauritanica(Apicomplexa: Adeleina: Haemogregarinidae) in captiveTestudo marginata (Reptilia: Testudinidae): Evidence for cyclic merogony? J Parasitol 2004, 90:1391-1393.
• [24]Mircean V, Dumitrache MO, Györke A, Pantchev N, Jodies R, Mihalca AD, Cozma V: Seroprevalence and geographic distribution of Dirofilaria immitis and tick-borne infections (Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Ehrlichia canis) in dogs from Romania. Vector Borne Zoonotic Dis 2012, 12:595-604.
• [25]Feider Z: Fauna RPR. Arachnida. Vol V. Fasc 2.. Bucureşti: Academiei RPR; 1965. in Romanian
• [26]Pleyer U, Priem S, Bergmann L, Burmester G, Hartmann C, Krause A: Detection of Borrelia burgdorferi DNA in urine of patients with ocular Lyme borreliosis. Br J Ophthalmol 2001, 85:552-555.
• [27]Courtney JW, Kostelnik LM, Zeidner NS, Massung RF: Multiplex Real-Time PCR for Detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 2004, 42:3164-3168.
• [28]Alsaleh A, Pellerin JL, Rodolakis A, Larrat M, Cochonneau D, Bruyas JF, Fieni F: Detection of Coxiella burnetii, the agent of Q fever, in oviducts and uterine flushing media and in genital tract tissues of the non pregnant goat. Comp Immunol Microb 2011, 34:355-360.
• [29]Rotondano TE, de Almeida AM, Lustosa EM, Cordeiro AA, Camboim EK, de Azvedo SS, de Andrade PP, de Melo MA: An assessment of whole blood and fractions by nested PCR as a DNA source for diagnosing canine ehrlichiosis and anaplasmosis. Scientific World Journal 2012, 2012:605743.
• [30]Rizzoli A, Hauffe HC, Carpi G, Vourc’h GI, Rosa R, Neteler M: Lyme borreliosis in Europe. Euro Surveill 2011, 16:1-8.
• [31]Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, Patz JA: Climate variability and change in the United States: potential impacts on vector and rodent-borne diseases. Environ Health Perspect 2001, 109:223-233.
• [32]Harrus S, Baneth G: Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases. Int J Parasitol 2005, 35:1309-1318.
• [33]Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS: Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 2010, 468:647-652.
• [34]Silaghi C, Woll D, Hamel D, Pfister K, Mahling M, Pfeffer M: Babesia spp. andAnaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents - Analyzing the host-pathogen-vector interface in a metropolitan area. Parasit Vectors 2012, 5:191. BioMed Central Full Text
• [35]Skuballa J, Petney T, Pfäffle M, Oehme R, Hartelt K, Fingerle V, Kimmig P, Taraschewski H: Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis, and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe. Ticks Tick Borne Dis 2012, 3:8-13.
• [36]Jaenson TGT, Hjertqvist M, Bergström T, Lundkvist Å: Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden. Parasit Vectors 2012, 5:184. BioMed Central Full Text
• [37]De Michelis S, Sewell HS, Collares-Pereira M, Santos-Reis M, Schouls LM, Benes V, Holmes EC, Kurtenbach K: Genetic diversity of Borrelia burgdorferi sensu lato in ticks from mainland Portugal. J Clin Microbiol 2000, 38:2128-2133.
• [38]Ekner A, Dudek K, Sajkowska Z, Majláthová V, Majláth I, Tryjanowski P: Anaplasmataceae andBorrelia burgdorferisensulato in the sand lizardLacerta agilis and co-infection of these bacteria in hostedIxodes ricinusticks. Parasit Vectors 2011, 4:182. BioMed Central Full Text
• [39]Tijsse-Klasen E, Fonville M, Reimerink JHJ, van der Sluijs Spitzen A, Sprong H: Role of sand lizards in the ecology of Lyme and other tick-borne diseases in the Netherlands. Parasit Vectors 2010, 3:42. BioMed Central Full Text
• [40]Eisen L, Lane RS: Vectors of Borrelia burgdorferi sensu lato. In Lyme Borreliosis: Biology, Epidemiology and Control. Wallingford, Oxon, UK: CABI Publishing; 2002:91-115.
• [41]Alleman AR, Wamsley HL: An update on anaplasmosis in dogs. Vet Med 2008, 103:212-220.
• [42]Smrdel KS, Serdt M, Duh D, Knap N, Zupanc TA: Anaplasma phagocytophilum in ticks in Slovenia. Parasit Vectors 2010, 3:102. BioMed Central Full Text
• [43]Nieto NC, Foley JE, Bettaso J, Lane RS: Reptile infection with Anaplasma phagocytophilum, the causative agent of granulocytic anaplasmosis. J Parasitol 2009, 95:1165-1170.
• [44]Nowak M, Cieniuch S, Stańczak J, Siuda K: Detection of Anaplasma phagocytophilum in Amblyomma flavomaculatum ticks (Acari: Ixodidae) collected from lizard Varanus exanthematicus imported to Poland. Exp Appl Acarol 2010, 51:363-371.
• [45]Torina A, Alongi A, Scimeca S, Vicente J, Caracappa S, de la Fuente J: Prevalence of tick-borne pathogens in ticks in Sicily. Transbound Emerg Dis 2010, 57:46-48.
• [46]Severinsson K, Jaenson TG, Pettersson J, Falk K, Nilsson K: Detection and prevalence of Anaplasma phagocytophilum and Rickettsia helvetica in Ixodes ricinus ticks in seven study areas in Sweden. Parasit Vectors 2010, 3:66. BioMed Central Full Text
• [47]Rikihisa Y: The tribe Ehrlichieae and ehrlichial diseases. Clin Microbiol Rev 1991, 4:286-308.
• [48]Torres FD: Biology and ecology of the brown dog tick,Rhipicephalus sanguineus. Parasit Vectors 2010, 3:26. BioMed Central Full Text
• [49]Maurin M, Raoult D: Q fever. Clin Microbiol Rev 1999, 12:518-553.
• [50]Kazar J: Coxiella burnetii infection. Ann N Y Acad Sci 2005, 1063:105-114.
• [51]Psaroulaki A, Ragiadakou D, Kouris G, Papadopoulos B, Chaniotis B, Tselentis Y: Ticks, tick-borne Rickettsiae, and Coxiella burnetii in the Greek Island of Cephalonia. Ann N Y Acad Sci 2006, 1078:389-399.
• [52]Řeháček J, Brezina R: Detection of Coxiella burnetii in saliva of experimentally infected ticks, Hyalomma dromedarii Koch. Bull World Health Organ 1968, 39:974-977.
• [53]Hirai K, To H: Advances in the understanding of Coxiella burnetii infection in Japan. J Vet Med Sci 1998, 60:781-790.
• [54]Murariu D: Mammal ecology and distribution from North Dobrogea (Romania). Travaux du Muséum National d’Histoire Naturelle «Grigore Antipa» 2006, 49:387-399.
• [55]Van den Brom R, Moll L, van Schaik G, Vellema P: Demography of Q fever seroprevalence in sheep and goats in The Netherlands in 2008. Prev Vet Medin press
• [56]Ardeleanu D, Neacşu GM, Pivoda CA, Enciu A: Poliparasitism structure in small ruminants in Dobrogea. Bull Univ Agri Sci Vet Med, Vet Med Book Ser 2003, 60:28-32. in Romanian