Hosein KHOVAND, Mohammad KHALILI, Maziar JAJARMI, SaeidReza NOUROLLAHIFARD

A survey of Ixodid ticks in stray dogs and molecular detection of Ehrlichia canis from ticks in central Iran

Ticks are well known as hematophagous ectoparasites, which cause different diseases in humans and animals. This investigation was designed in central Iran to assess the prevalence, intensity, and abundance of tick infestation in stray dogs and detection of Ehrlichia canis. Overall, 962 ticks were collected from 260 stray dogs between April and August 2018. DNA samples with the goal of amplification of pathogen were screened by real-time PCR assay. The prevalence of tick infestation on stray dogs was 60.3%. Rhipicephalus sanguineus sensu lato (s.l.) was only species found in stray dogs. Out of 42 tick pools, 4 (9.5%) were positive for E. canis in real-time PCR assay. This study showed the presence of E. canis for the first time in ticks infesting stray dogs in central Iran and proved that these ticks can emerge as a zoonotic disease.

PDF

___

1. Saleh MN, Sundstrom KD, Duncan KT, Ientile MM, Jordy J et al. Show us your ticks: a survey of ticks infesting dogs and cats across the USA. Parasites & Vectors 2019; 12 (1): 1-11. doi: 10.1186/s13071-019-3847-3
2. Ebrahimzade E, Fattahi R, Ahoo MB. Ectoparasites of stray dogs in Mazandaran, Gilan and Qazvin Provinces, North and center of Iran. Journal of Arthropod-Borne Diseases 2016; 10 (3): 364-369.
3. Beck S, Schreiber C, Schein E, Krücken J, Baldermann C et al. Tick infestation and prophylaxis of dogs in northeastern Germany: a prospective study. Ticks & Tick-Borne Diseases 2014; 5 (3): 336-342. doi: 10.1016/j.ttbdis.2013.12.009
4. Sahu A, Mohanty B, Panda MR, Sardar KK, Dehuri M. Prevalence of tick infestation in dogs in and around Bhubaneswar. Veterinary World 2013; 6 (12): 982-985. doi: 10.14202/vetworld.2013.982-985
5. Schreiber C, Krücken J, Beck S, Maaz D, Pachnicke S et al. Pathogens in ticks collected from dogs in Berlin/Brandenburg, Germany. Parasites & Vectors 2014; 7 (1): 1-10. doi: 10.1186/ s13071-014-0535-1
6. Dantas-Torres F. Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasites & Vectors 2010; 3 (1): 1-11. doi: 10.1186/1756-3305-3-26
7. Akande FA, Adebowale AF, Idowu OA, Sofela OO. Prevalence of ticks on indigenous breed of hunting dogs in Ogun state, Nigeria. Sokoto Journal of Veterinary Sciences 2018; 16 (3): 66- 71. doi: 10.4314/sokjvs.v16i3.10
8. Vasquez A, Goolsby JA, Vacek AT, Racelis A, Kariyat RR. Incidence of the Brown dog tick, Rhipicephalus sanguineus and its parasitoid, Ixodiphagus hookeri on dogs in South Texas. Subtropical Agriculture & Environments 2019; 70: 6-10.
9. Otranto D, Dantas-Torres F, Breitschwerdt EB. Managing canine vector-borne diseases of zoonotic concern: part one. Trends in Parasitology 2009; 25 (4): 157-163. doi: 10.1016/j. pt.2009.01.003
10. Harrus S, Waner T. Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): an overview. The Veterinary Journal 2011; 187 (3): 292-296. doi: 10.1016/j.tvjl.2010.02.001
11. Cetinkaya H, Matur E, Akyazi I, Ekiz EE, Aydin L et al. Serological and molecular investigation of Ehrlichia spp. and Anaplasma spp. in ticks and blood of dogs, in the Thrace Region of Turkey. Ticks & Tick-borne Diseases 2016; 7 (5): 706-714. doi: 10.1016/j.ttbdis.2016.02.021
12. Malik MI, Qamar M, Ain Q, Hussain MF, Dahmani M et al. Molecular detection of Ehrlichia canis in dogs from three districts in Punjab (Pakistan). Veterinary Medicine & Science 2018; 4 (2): 126-132. doi: 10.1002/vms3.94
13. Bastos AD, Mohammed OB, Bennett NC, Petevinos C, Alagaili AN. Molecular detection of novel Anaplasmataceae closely related to Anaplasma platys and Ehrlichia canis in the dromedary camel (Camelus dromedarius). Veterinary Microbiology 2015; 179 (3-4): 310-314. doi: 10.1016/j.vetmic.2015.06.001
14. Zaid T, Ereqat S, Nasereddin A, Al‐Jawabreh A, Abdelkader A et al. Molecular characterization of Anaplasma and Ehrlichia in ixodid ticks and reservoir hosts from Palestine: a pilot survey. Veterinary Medicine & Science 2019; 5 (2): 230-242. doi: 10.1002/vms3.150
15. Gal A, Loeb E, Yisaschar-Mekuzas Y, Baneth G. Detection of Ehrlichia canis by PCR in different tissues obtained during necropsy from dogs surveyed for naturally occurring canine monocytic ehrlichiosis. The Veterinary Journal 2008; 175(2):212-217. doi: 10.1016/j.tvjl.2007.01.013
16. Foongladda S, Inthawong D, Kositanont U, Gaywee J. Rickettsia, Ehrlichia, Anaplasma, and Bartonella in ticks and fleas from dogs and cats in Bangkok. Vector-Borne & Zoonotic Diseases 2011; 11 (10): 1335-1341. doi: 10.1089/vbz.2010.0174
17. Ybañez AP, Perez ZO, Gabotero SR, Yandug RT, Kotaro M et al. First molecular detection of Ehrlichia canis and Anaplasma platys in ticks from dogs in Cebu, Philippines. Ticks & Tick-Borne Diseases 2012; 3 (5-6): 288-293. doi: 10.1016/j. ttbdis.2012.10.032
18. Nazari M, Lim SY, Watanabe M, Sharma RS, Cheng NA et al. Molecular detection of Ehrlichia canis in dogs in Malaysia. Plos Neglected Tropical Diseases 2013; 7 (1): 1-4. doi: 10.1371/ journal.pntd.0001982
19. Koh FX, Panchadcharam C, Tay ST. Vector-borne diseases in stray dogs in peninsular Malaysia and molecular detection of Anaplasma and Ehrlichia spp. from Rhipicephalus sanguineus (Acari: Ixodidae) ticks. Journal of Medical Entomology 2016; 53 (1): 183-187. doi: 10.1093/jme/tjv153
20. Haryanto A, Tjahajati I. Molecular characterization and blood hematology profile of dogs infected by Ehrlichia canis in Yogyakarta, Indonesia. Biodiversitas Journal of Biological Diversity 2020; 21 (7): 3242-3248. doi: 10.13057/biodiv/ d210746
21. Akhtardanesh B, Ghanbarpour R, Blourizadeh H. Serological evidence of canine monocytic ehrlichiosis in Iran. Comparative Clinical Pathology 2010; 19 (5): 469-474. doi: 10.1007/s00580- 009-0889-5
22. Ipek Neval DS, Özübek S, Aktas M. Molecular Evidence for Transstadial Transmission of Ehrlichia canis by Rhipicephalus sanguineus sensu lato Under Field Conditions. Journal of Medical Entomology 2018; 55(2): 440–444. doi.org/10.1093/ jme/tjx217
23. Baneth G, Harrus S, Ohnona FS, Schlesinger Y. Longitudinal quantification of Ehrlichia canis in experimental infection with comparison to natural infection. Veterinary Microbiology 2009; 136 (3-4): 321-325. doi: 10.1016/j.vetmic.2008.11.022
24. Masala G, Chisu V, Foxi C, Socolovschi C, Raoult D et al. First detection of Ehrlichia canis in Rhipicephalus bursa ticks in Sardinia, Italy. Ticks & Tick-Borne Diseases 2012; 3 (5-6): 396- 397. doi: 10.1016/j.ttbdis.2012.10.006
25. Dahmani M, Davoust B, Rousseau F, Raoult D, Fenollar F et al. Natural Anaplasmataceae infection in Rhipicephalus bursa ticks collected from sheep in the French Basque Country. Ticks &Tick-Borne Diseases 2017; 8 (1): 18-24. doi: 10.1016/j. ttbdis.2016.09.009
26. Hornok S, Fuente J, Horváth G, Fernández de Mera I, Wijnveld M et al. Molecular evidence of Ehrlichia canis and Rickettsia massiliae in ixodid ticks of carnivores from South Hungary. Acta Veterinaria Hungarica 2013; 61 (1): 42-50. doi: 10.1556/ avet.2012.050
27. Sanches GS, Couto J, Silva-Pedrosa R, Ferrolho J, Santos AS et al. Molecular heterogeneity of Rhipicephalus sanguineus sensu lato and screening for Ehrlichia canis in mainland Portugal. Ticks & Tick-Borne Diseases 2018; 9 (6): 1383-1390. doi: 10.1016/j.ttbdis.2018.06.002
28. Kang SW, Doan HT, Choe SE, Noh JH, Yoo MS et al. Molecular investigation of tick-borne pathogens in ticks from grazing cattle in Korea. Parasitology International 2013; 62 (3): 276- 282. doi: 10.1016/j.parint.2013.02.002
29. Khazeni A, Telmadarraiy Z, Oshaghi MA, Mohebali M, Zarei Z et al. Molecular detection of Ehrlichia canis in ticks’ population collected on dogs in Meshkin-Shahr, Ardebil Province, Iran. Journal of Biomedical Science & Engineering 2013; 6: 1-5. doi: 10.4236/jbise.2013.67A3001
30. Walker AR. Ticks of Domestic Animals in Africa: a guide to identification of species. 1st ed. Edinburgh: Bioscience Reports; 2003. pp. 3-210.
31. Doyle CK, Labruna MB, Breitschwerdt EB, Tang YW, Corstvet RE et al. Detection of medically important Ehrlichia by quantitative multicolor TaqMan real-time polymerase chain reaction of the dsb gene. The Journal of Molecular Diagnostics 2005; 7 (4): 504-510. doi: 10.1016/S1525-1578(10)60581-8
32. Bahrami AM, Doosti A, Ahmady Asbchin S. Cat and dogs’ ectoparasite infestations in Iran and Iraq border line area. World Applied Sciences Journal 2012; 18 (7): 884-889. doi: 10.5829/idosi.wasj.2012.18.07.1376
33. Mosallanejad B, Alborzi AR, Katvandi N. A survey on ectoparasite infestations in companion dogs of Ahvaz district, south-west of Iran. Journal of Arthropod-Borne Diseases 2012; 6 (1): 70-78.
34. Memon MA, Arijo AG, Rajput ZI, Akhter N. Documentation and magnitude of ticks infesting dogs in Karachi. Pakistan Journal of Parasitology 2017; 63: 33-46.
35. Opeyemi OA, Babamale OA, Shittu O, Mohammad MU, Ugbomoiko US. Seasonal distribution and common management practices of ectoparasites of domestic dogs in Ilorin, Nigeria. Animal Research International 2019; 16 (1): 3265-3272.
36. Chao LL, Hsieh CK, Ho TY, Shih CM. First zootiological survey of hard ticks (Acari: Ixodidae) infesting dogs in northern Taiwan. Experimental & Applied Acarology 2019; 77 (1): 105-115. doi: 10.1007/s10493-018-0328-x
37. Hassissen L, Kebbi R, Ayad A, Nait-Mouloud M. Seasonal activity of ticks infesting domestic dogs in Bejaia province, Northern Algeria. Onderstepoort Journal of Veterinary Research 2019; 86 (1):1-6. doi: 10.4102/ojvr.v86i1.1755
38. Dantas-Torres F. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Veterinary Parasitology 2008; 152 (3-4): 173-185. doi: 10.1016/j.vetpar.2007.12.030
39. Abuzeid AM, Sallam NH, Youssef EM, El‐Gayar AK, Abdel Aal AA et al. Studies on ectoparasites of stray dogs in Ismailia City. Egyptian Veterinary Medical Society of Parasitology Journal 2015; 11 (1): 115-122. doi: 10.21608/evmspj.2015.38000
40. Shitta KB, James-Rugu NN, Badaki JA. Prevalence of ticks on dogs in Jos, Plateau State, Nigeria. Bayero Journal of Pure & Applied Sciences 2018; 11 (1): 451-454. doi: 10.4314/bajopas. v11i1.71S
41. Arong GA, Shitta KB, James-Rugu NN, Effanga EO. Seasonal variation in the abundance and distribution of ixodid ticks on mongrel, alsatian and mixed breeds of dogs (Canis familiaris) in Jos, in plateau state, north-central Nigeria. World Journal of Science & Technology 2011; 1(4):24-29.
42. Hadi UK, Soviana S, Pratomo IR. Prevalence of ticks and tick-borne diseases in Indonesian dogs. Journal of Veterinary Science & Technology 2016; 7(3): 1-7.
43. Maurelli MP, Pepe P, Colombo L, Armstrong R, Battisti E et al. A national survey of Ixodidae ticks on privately owned dogs in Italy. Parasites & Vectors 2018; 11 (1): 1-10. doi: 10.1186/ s13071-018-2994-2
44. Tinoco-Gracia L, Quiroz-Romero H, Quintero-Martínez MT, Rentería-Evangelista TB, González-Medina Y et al. Prevalence of Rhipicephalus sanguineus ticks on dogs in a region on the Mexico-USA border. The Veterinary Record 2009; 164 (2): 59- 61.
45. Ndip LM, Ndip RN, Esemu SN, Walker DH, McBride JW. Predominance of Ehrlichia chaffeensis in Rhipicephalus sanguineus ticks from kennel-confined dogs in Limbe, Cameroon. Experimental & Applied Acarology 2010; 50 (2): 163-168. doi: 10.1007/s10493-009-9293-8
46. Derakhshandeh N, Sharifiyazdi H, Hasiri MA. Molecular detection of Ehrlichia spp. in blood samples of dogs in southern Iran using polymerase chain reaction. Veterinary Research Forum 2017; 8 (4): 347-351.
47. Gaunt SD, Beall MJ, Stillman BA, Lorentzen L, Diniz PP et al. Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: hematologic, serologic and molecular findings. Parasites & vectors 2010; 3 (33): 1-10. doi: 10.1186/1756-3305-3-33
48. Aguiar DM, Cavalcante GT, Pinter A, Gennari SM, Camargo LM et al. Prevalence of Ehrlichia canis (Rickettsiales: Anaplasmataceae) in dogs and Rhipicephalus sanguineus (Acari: Ixodidae) ticks from Brazil. Journal of Medical Entomology 2007; 44 (1): 126-132. doi: 10.1093/jmedent/41.5.126
49. Perez M, Bodor M, Zhang C, Xiong Q, Rikihisa Y. Human infection with Ehrlichia canis accompanied by clinical signs in Venezuela. Annals of the New York Academy of Sciences 2006; 1078 (1): 110-117. doi: 10.1196/annals.1374.016
50. Vieira RF, Vieira TS, Nascimento DD, Martins TF, Krawczak FS et al. Serological survey of Ehrlichia species in dogs, horses and humans: zoonotic scenery in a rural settlement from southern Brazil. Revista do Instituto de Medicina Tropical de São Paulo 2013; 55 (5): 335-340. doi: 10.1590/S0036-46652013000500007
51. Bouza-Mora L, Dolz G, Solórzano-Morales A, Romero-Zuñiga JJ, Salazar-Sánchez L et al. Novel genotype of Ehrlichia canis detected in samples of human blood bank donors in Costa Rica. Ticks and Tick-Borne Diseases 2017; 8 (1): 36-40. doi: 10.1016/j.ttbdis.2016.09.012
52. Babamahmoodi F. First outbreak of human ehrlichiosis in Mazandaran Province. In: proceedings of the 12th Iranian Congress of Tropical Infectious Disease; Tehran, Iran; 2004. pp. 17-21.