Identification of Hepatozoon and Cercopithifilaria in ticks infesting dogs of different regions of Iran

Document Type : Paper, Persian

Authors

1 Department of Pathobiology, Faculty of Veterinary Science, Bu-Ali Sina University, Hamedan, Iran

2 Department of Veterinary Medicine, University of Bari, Bari, Italy

10.52547/JESI.43.1.6

Abstract

Following previous detection of Hepatozoon canis and Cercopithifilaria bainae in dogs from Iran, this study aimed to identify potential tick vectors collected from dogs from five provinces of Iran. From October 2018 to September 2021, a total of 222 owned and 541 sheltered dogs from Hamedan (n=305), Kermanshah (n = 227), Yazd (n =80), Khouzestan (n =71), and Mazandaran (n =80) were examined for ticks. Collected ticks (n =3339) were identified morphologically, and adults were screened for the detection of Hepatozoon and Cercopithifilaria either with conventional PCR (n=119 ticks), tick dissection (n=106), or microscopical examination after fixation in formalin (n =102). A total of 169 dogs (22.1%) were infested with ticks. Tick infestation rate varied in different provinces (i.e., 32.4% in Hamedan, 27.3% in Kermanshah, 10.0% in Yazd), but no ticks were collected in dogs from Mazandaran and Khouzestan. The majority of male ticks were identified as Rhipicephalus sanguineus sensu lato (89.3%) and Rhipicephalus turanicus, but one dog from Kermanshah was infested with Hyalomma asiaticum (1 male and 1 female) and Hyalomma excavatum (1 male). At the molecular examination, Cercopithifilaria was detected in 14.28%, Hepatozoon in 6.7% ticks, and both parasites in 1.68% of Rhipicephalus ticks. Parasites were not observed at tick dissection and histological examinations. Nucleotide sequencing and phylogenetic analyses revealed C. bainae and H. canis in R. sanguineus sensu lato and R. turanicus ticks. Data suggests that both tick species above may play a role in the epidemiology of Cercopithifilaria and Hepatozoon in Iran.
 
 

Graphical Abstract

Identification of  Hepatozoon and  Cercopithifilaria in ticks infesting dogs of different regions of Iran

Keywords

Main Subjects


 © 2023 by Author(s), Published by the Entomological Society of Iran

This Work is Licensed under Creative Commons Attribution-Non Commercial 4.0 International Public License

انی آلودگی به کنه و نیز فون کنه­های سگ­ در بسیاری از نقاط کشور تاکنون نامشخص است برنامه­ریزی جهت مطالعات گسترده­ی اپیدمیولوژیک در یک بازه­ی زمانی معین ضروری به نظر می­رسد.
نتیجه­گیری
مطالعه­ی حاضر نشان­ دهنده­ی نقش کنه­های ­Rhipicephalus sanguineus و Rhipicephalus turanicus­ در اپیدمیولوژی انگل­های Cercopithifilaria bainae و Hepatozoon canis در ایران است. جهت محافظت سگ­ها از کنه­زدگی و متعاقباً بروز بیماری­های کنه­زاد ازجمله سرکوپیتی­فیلاریوزیس و هپاتوزوئونوزیس استفاده از داروها و سموم مؤثر و نیز قلاده­های ضدانگل خارجی پیشنهاد می­گردد.
 
Amoli, A., Rahmani, A., Khoshnegah, J. & Razmi, Gh. R. (2012) A preliminary parasitological survey of Hepatozoon spp. infection in dogs in Mashhad, Iran. Iranian Journal of Parasitology 7(4), 99-103.
Angelou, A., Latrofa, M. S., Annoscia, G., Symeonidou, I., Theodoridis, A., Polizopoulou, Z. S., Otranto, D. & Papadopoulos, E. (2020) Cercopithifilaria species in dogs and ticks from Greece. Parasitology Research 119(10), 3391-3400. doi: https://doi.org/10.1007/s00436-020-06784-3
Bahrami, A. M., Doosti, A. & Ahmady Asbchin, S. (2012) Cat and dogs ectoparasite infestations in Iran and Iraq boarder line area. World Applied Sciences Journal 18(7), 884-889.https://doi.org/10.5829/idosi.wasj.2012.18.07.1376
Baneth, G., Samish, M., Aleksefv, E., Aroch, I. & Shkap, V. (2001) Transmission of Hepatozoon canis to dogs by naturally-fed or percutaneously-injected Rhipicephalus sanguineus ticks. Journal of Parasitology 87(3), 606-611. https://doi.org/10.1645/0022-3395(2001)087[0606:TOHCTD]2.0.CO;2
Baneth, G., Samish, M. & Shkap, V. (2007) Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). Journal of Parasitology 93(2), 283-299. https://doi.org/10.1645/GE-494R.1
Bezerra-Santos, M. A., de Macedo, L. O., Nguyen, V. L., Manoj, R. R. S., Laidoudi, Y., Latrofa, M. S., Beugnet, F. & Otranto, D. (2022) Cercopithifilaria spp. in ticks of companion animals from Asia: new putative hosts and vectors. Ticks and Tick-borne Diseases 13(4), 101957. https://doi.org//doi.org/10.1016/j.ttbdis.2022.101957
Brianti, E., Otranto, D., Dantas-Torres, F., Weigl, S., Latrofa, M. S., Dantas-Torres, F., Giannelli, A., Gaglio, G., Napoli, E., Brucato, G., Cauquil, L. & Giannetto, S. (2012) Rhipicephalus sanguineus (Ixodida, Ixodidae) as intermediate host of a canine neglected filarial species with dermal microfilariae. Veterinary Parasitology 183(3-4), 330-337. https://doi.org/10.1016/j.vetpar.2011.07.031
Casiraghi, M., Anderson, T. J. C., Bandi, C., Bazzocchi, C. & Genchi, C. (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122(1), 93-103. https://doi.org/10.1017/s0031182000007149
Dantas-Torres, F. (2008) The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806)(Acari: Ixodidae): from taxonomy to control. Veterinary Parasitology 152(3-4), 173-185. https://doi.org/10.1016/j.pt.2022.08.011
Dantas-Torres, F. (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasites and Vectors 3(1), 26. https://doi.org/doi.org/10.1186/1756-3305-3-26
Dantas-Torres, F., Latrofa, M. S., Weigl, S., Tarallo, V. D., Lia, R. P. & Otranto, D. (2011) Hepatozoon canis infection in ticks during spring and summer in Italy. Journal of Parasitology 93(2), 283-299. https://doi.org/10.1007/s00436-011-2544-8
Dantas-Torres, F. & Otranto, D. (2022) Rhipicephalus sanguineus (Brown dog tick). Trends in Parasitology 38(11), 993-994.  https://doi.org//doi.org/10.1016/j.pt.2022.08.011
De Miranda, R. L., de Castro, J. R., Olegário, M. M. M., Beletti, M. E., Mundim, A. V., O’Dwyer, L. H., Eyal, O., Talmi-Frank, D., Cury, M. C. & Baneth, G. (2011) Oocysts of Hepatozoon canis in Rhipicephalus (Boophilus) microplus collected from a naturally infected dog. Veterinary Parasitology 177(3-4), 392-396. https://doi.org/10.1016/j.vetpar.2011.01.044
Ebrahimzade, E., Fattahi, R. & Ahoo, M. B. (2016) Ectoparasites of stray dogs in Mazandaran, Gilan and Qazvin Provinces, North and center of Iran. Journal of Arthropod-Borne Diseases 10(3), 366-371.
Estrada-Peña, A., Mihalca, A. D. & Petney, T. N. (2017) Ticks of Europe and North Africa: A Guide to Species Identification (A. Estrada-Peña, Mihalca, A. D.,  Petney, T. N., Ed. 1st ed. ed.). Springer. 10.1007/978-3-319-63760-0
Gabrielli, S., Giannelli, A., Brianti, E., Dantas-Torres, F., Bufalini, M., Fraulo, M., La-Torre Ramos, F. R. A. N., Cantacessi, C., Latrofa, M. S., Cancrini, G. & Otranto, D. (2014) Chronic polyarthritis associated to Cercopithifilaria bainae infection in a dog. Veterinary Parasitology 205(1-2), 401-404. https://doi.org/10.1016/j.vetpar.2014.06.027
Giannelli, A., Lia, R. P., Annoscia, G., Buonavoglia, C., Lorusso, E., Dantas-Torres, F., Baneth, G. & Otranto, D. (2017) Rhipicephalus turanicus, a new vector of Hepatozoon canis. Parasitology 144(6), 730-737.
Hodžić, A., Alić, A., Fuehrer, H. P., Harl, J., Wille-Piazzai, W. & Duscher, G. G. (2015) A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasites & Vectors 8(1), 88-88. https://doi.org/10.1186/s13071-015-0692-x
Hosseini-Chegeni, A., Tavakoli, M. & Telmadarraiy, Z. (2019) The updated list of ticks (Acari: Ixodidae & Argasidae) occurring in Iran with a key to the identification of species. Systematic and Applied Acarology 24(11), 2133-2166. https://doi.org/10.11158/saa.24.11.8
Iatta, R., Sazmand, A., Nguyen, V. L., Nemati, F., Bahiraei, Z., Mazhar Ayaz, M., Giannico, A., Dantas-Torres, F. & Otranto, D. (2021) Vector-borne pathogens in dogs of different regions of Iran and Pakistan. Parasitology Research 120(12), 4219-4228. https://doi.org/10.1007/s00436-020-06992-x
Ionică, A. M., D’Amico, G., Mitková, B., Kalmár, Z., Annoscia, G., Otranto, D., Modri, D. & Mihalca, A. D. (2014) First report of Cercopithifilaria spp. in dogs from Eastern Europe with an overview of their geographic distribution in Europe. Parasitology Research 113(7), 2761-2764. https://doi.org//doi.org/10.1007/s00436-014-3931-8
Jafari-Shoorijeh, S., Rowshan-Ghasrodashti, A., Tamadon, A., Moghaddar, N. & Behzadi, M. A. (2008) Seasonal frequency of ectoparasite infestation in dogs from Shiraz, Southern Iran. Turkish Journal of Veterinary and Animal Sciences 32(4), 309-313.
Jamshidi, S., Maazi, N., Ranjbar-Bahadori, S., Rezaei, M., Morakabsaz, P. & Hosseininejad, M. (2012) A survey of ectoparasite infestation in dogs in Tehran, Iran. Revista Brasileira de Parasitologia Veterinária 21(3), 326. https://doi.org/10.1590/S1984-29612012000300030 
Khazeni, A., Telmadarraiy, Z., Oshaghi, M. A., Mohebali, M., Zarei, Z. & Abtahi, S. M. (2013) Molecular detection of Ehrlichia canis in ticks population collected on dogs in Meshkin-Shahr, Ardebil Province, Iran. Journal of Biomedical Science and Engineering 6, 1-5. http://dx.doi.org/10.4236/jbise.2013.67A3001
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7), 1870-1874. https://doi.org/10.1093/molbev/msw054
Lade, B., Patil, A. & Paikrao, H. (2014) Efficient genomic DNA extraction protocol from medicinal rich Passiflora foetida containing high level of polysaccharide and polyphenol. SpringerPlus 3(1), 1-7. https://doi.org/10.1186/2193-1801-3-457
Latrofa, M. S., Dantas-Torres, F., Giannelli, A. & Otranto, D. (2014) Molecular detection of tick-borne pathogens in Rhipicephalus sanguineus group ticks. Ticks and Tick-borne Diseases 5(6), 943-946. https://doi.org/10.1016/j.actatropica.2022.106582
Latrofa, M. S., Weigl, S., Dantas-Torres, F., Annoscia, G., Traversa, D., Brianti, E. & Otranto, D. (2012) A multiplex PCR for the simultaneous detection of species of filarioids infesting dogs. Acta Tropica 122(1), 150-154. https://doi.org/10.1016/j.actatropica.2012.01.006
Maia, C., Casero, M., Annoscia, G., Latrofa, M. S., Colella, V., Pereira, A., Azevedo, F. & Otranto, D. (2017) Cercopithifilaria sp. II in Vulpes vulpes: new host affiliation for an enigmatic canine filarioid. Parasitology Research 116(1), 441-443. https://doi.org/10.1007/s00436-016-5308-7
Manoj, R. R. S., Iatta, R., Latrofa, M. S., Capozzi, L., Raman, M., Colella, V. & Otranto, D. (2020) Canine vector-borne pathogens from dogs and ticks from Tamil Nadu, India. Acta Tropica 203, 105308. https://doi.org/10.1016/j.actatropica.2019.105308
Minabaji, A., Moshaverinia, A. & Khoshnegah, J. (2020) Frequency of ectoparasite infestation in dogs in Mashhad, Northeast Iran. Journal of Veterinary Research 75(3), 280-287. https://doi.org/10.22059/jvr.2019.274542.2894
Mirani, F., Yakhchali, M. & Naem, S. (2017) A study on ectoparasites fauna of dogs in suburbs of Ghilanegharb, Kermanshah province, Iran. Journal of Faculty of Veterinary Medicine University of Tehran 72(1), 7-14 [Article in Persian with English abstract]. https://doi.org/10.22059/jvr.2017.61285
Mosallanejad, B., Alborzi, A. R. & Katvandi, N. (2012) A Survey on ectoparasite infestations in companion dogs of Ahvaz District, South-west of Iran. Jornal of Arthropod-Borne Diseases 6(1), 70-78.
Murata, T., Inoue, M., Taura, Y., Nakama, S., Abe, H. & Fujisaki, K. (1995) Detection of Hepatozoon canis oocyst from ticks collected from the infected dogs. Journal of Veterinary Medical Science 57(1), 111-112. https://doi.org/10.22092/ari.2017.110293.1125
Nava, S., Beati, L., Venzal, J. M., Labruna, M. B., Szabó, M. P., Petney, T., Saracho-Bottero, M. N., Tarragona, E. L., Dantas-Torres, F. & Silva, M. M. S. (2018) Rhipicephalus sanguineus (Latreille, 1806): Neotype designation, morphological re-description of all parasitic stages and molecular characterization. Ticks and Tick-borne Diseases 9(6), 1573-1585. https://doi.org//doi.org/ 10.1016/j.ttbdis.2018.08.001
O’Dwyer, L. H. (2011) Brazilian canine hepatozoonosis. Revista Brasileira de Parasitologia Veterinária 20(3) 181-193. https://doi.org/10.1590/s1984-29612011000300002
Otranto, D., Brianti, E., Abramo, F., Gaglio, G., Napoli, E., Latrofa, M. S., Ramos, R. A., Dantas-Torres, F. & Bain, O. (2012) Cutaneous distribution and localization of Cercopithifilaria sp. microfilariae in dogs. Veterinary Parasitology 190(1-2), 143-150. https://doi.org/10.1016/j.vetpar.2012.05.016
Otranto, D., Brianti, E., Dantas-Torres, F., Miro, G., Latrofa, M. S., Mutafchiev, Y. & Bain, O. (2013) Species diversity of dermal microfilariae of the genus Cercopithifilaria infesting dogs in the Mediterranean region. Parasitology 140(1) 99-108. https://doi.org/10.1017/S0031182012001357
Otranto, D., Brianti, E., Latrofa, M. S., Dantas-Torres, F., Giannelli, A., Annoscia, G., Weigl, S., Lia, R. P., Gaglio, G., Napoli, E., Giannetto, S. & Papadopoulos, E. (2012) On a Cercopithifilaria sp. transmitted by Rhipicephalus sanguineus: a neglected, but widespread filarioid of dogs. Parasites & Vectors 5(1), 1.  https://doi.org/10.1186/1756-3305-5-1
Otranto, D., Huchet, J. B., Giannelli, A., Callou, C. & Dantas-Torres, F. (2014) The enigma of the dog mummy from Ancient Egypt and the origin of ‘Rhipicephalus sanguineus’. Parasites & Vectors 7, 2. https://doi.org/10.1186/1756-3305-7-2
Otranto, D., Varcasia, A., Solinas, C., Scala, A., Brianti, E., Dantas-Torres, F., Annoscia, G., Martin, C., Mutafchiev, Y. & Bain, O. (2013) Redescription of Cercopithifilaria bainae Almeida & Vicente, 1984 (Spirurida, Onchocercidae) from a dog in Sardinia, Italy. Parasites and Vectors 6(1), 132. https://doi.org/doi.org/10.1186/1756-3305-6-132
Petit, G., Bain, O., Cassone, J. & Seureau, C. (1988) La filaire Cercopithifilaria roussilhonichez la tique vectrice. Annales de Parasitologie Humaine et Comparée 63(4), 296-302. https://doi.org/doi:10.1051/parasite/1988634296
Ramos, R. A. N., Giannelli, A., Lia, R. P., Brianti, E., Tarallo, V. D., Breitshwerdt, E. B., Dantas-Torres, F., Stanneck, D. & Otranto, D. (2014) Incidence of Cercopithifilaria bainae in dogs and probability of co-infection with other tick-borne pathogens. PLoS One 9(2), e88198. http://dx.doi.org/10.1371/journal.pone.0088198
Ramos, R. A. N., Giannelli, A., Brianti, E., Annoscia, G., Cantacessi, C., Dantas-Torres, F. & Otranto, D. (2013) Tick vectors of Cercopithifilaria bainae in dogs: Rhipicephalus sanguineus sensu lato versus Ixodes ricinus. Parasitology Research 112(8), 3013-3017. https://doi.org/10.1007/s00436-013-3474-4
Santos, M. A. B., de Macedo, L. O., Otranto, D., do Nascimento Ramos, C. A., do Rêgo, A. G. d. O., Giannelli, A., Alves, L. C., de Carvalho, G. A. & Ramos, R. A. N. (2018) Screening of Cercopithifilaria bainae and Hepatozoon canis in ticks collected from dogs of Northeastern Brazil. Acta Parasitologica 63(3), 605-608. https://doi.org/10.1515/ap-2018-0069
Sazmand, A., Bahiraei, Z., Nemati, F., Annoscia, G., Bezerra-Santos, M. A., Nayebzadeh, H., Salemi, A. M., Mousavi, S. M., Sajjadi, S. M. & Otranto, D. (2022) Dermal microfilariae of dogs, jackals and cats in different regions of Iran. Parasites & Vectors 15, 28. https://doi.org/10.1186/s13071-021-05141-2
Shamshiri, Z., Goudarztalejerdi, A., Zolhavarieh, S. M., Kamalpour, M. & Sazmand, A. (2022) Molecular Identification of Bartonella species in dogs and arthropod vectors in Hamedan and Kermanshah, Iran. Iranian Veterinary Journal, In-Press. https://doi.org/10.22055/ivj.2022.325115.2436
Šlapeta, J., Chandra, S. & Halliday, B. (2021) The “tropical lineage” of the brown dog tick Rhipicephalus sanguineus sensu lato identified as Rhipicephalus linnaei. International Journal for Parasitology 51(6), 431-436. https://doi.org/10.1016/j.ijpara.2021.02.001
Šlapeta, J., Halliday, B., Chandra, S., Alanazi, A. D. & Abdel-Shafy, S. (2022) Rhipicephalus linnaei (Audouin, 1826) recognised as the “tropical lineage” of the brown dog tick Rhipicephalus sanguineus sensu lato: neotype designation, redescription, and establishment of morphological and molecular reference. Ticks and Tick-borne Diseases 102024. http://dx.doi.org/10.1016/j.ttbdis.2018.08.001
Šlapeta, J., Halliday, B., Dunlop, J. A., Nachum-Biala, Y., Salant, H., Ghodrati, S., Modrý, D. & Harrus, S. (2023) The “southeastern Europe” lineage of the brown dog tick Rhipicephalus sanguineus (sensu lato) identified as Rhipicephalus rutilus Koch, 1844: Comparison with holotype and generation of mitogenome reference from Israel. Current Research in Parasitology & Vector-borne Diseases, 3, 100118. https://doi.org/10.1016/j.crpvbd.2023.100118
Soltani, R. & Dalimi, A. (2018) A molecular study on Hepatozoon canis infection in dogs in Tehran (Iran). Archives of Razi Institute 73(4), 257-263. https://doi.org/10.22092/ari.2017.110293.1125
Uni, S., Bain, O., Fujita, H., Matsubayashi, M., Fukuda, M. & Takaoka, H. (2013) Infective larvae of Cercopithifilaria spp. (Nematoda: Onchocercidae) from hard ticks (Ixodidae) recovered from the Japanese serow (Bovidae). Parasite 20(1), 1-7. http://dx.doi.org/10.1051/parasite/2012001
Walker, J. B., Keirans, J. E. & Horak, I. G. (2000) The Genus Rhipicephalus (Acari, Ixodidae): A Guide to the Brown Ticks of the World Revised, Cambridge University Press. https://doi.org/doi.org/10.1017/CBO9780511661754
Zintl, A., Finnerty, E. J., Murphy, T. M., de Waal, T. & Gray, J. S. (2011) Babesias of red deer (Cervus elaphus) in Ireland. Veterinary Research 42(1), 7. https://doi.org/10.1186/1297-9716-42-7