Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T06:58:08.391Z Has data issue: false hasContentIssue false

Filarial worms: a systematic review and meta-analysis of diversity in animals from Iran with emphasis on human cases

Published online by Cambridge University Press:  06 April 2020

Ezatollah Ghasemi
Affiliation:
Department of Medical Parasitology, School of Medicine, Dezful University of Medical Sciences, Dezful, Iran
Sadegh Shamsinia
Affiliation:
Faculty of Medical Sciences, Department of Parasitology, Tarbiat Modares University, Tehran, Iran
Ali Taghipour
Affiliation:
Faculty of Medical Sciences, Department of Parasitology, Tarbiat Modares University, Tehran, Iran
Davood Anvari
Affiliation:
Department of Parasitology, Student Research Committee, Mazandaran University of Medical Sciences, Sari, Iran School of Medicine, Iranshahr University of Medical Sciences, Iranshahr, Iran
Saeed Bahadory
Affiliation:
Faculty of Medical Sciences, Department of Parasitology, Tarbiat Modares University, Tehran, Iran
Seyyed Ali Shariatzadeh
Affiliation:
Department of Parasitology, Student Research Committee, Mazandaran University of Medical Sciences, Sari, Iran
Bahareh Kordi
Affiliation:
Department of Basic Medical Sciences, Neyshabur University of Medical Sciences, Neyshabur, Iran Faculty of Veterinary Medicine, Department of Pathobiology, Ferdowsi University of Mashhad, Mashhad, Iran
Hamidreza Majidiani*
Affiliation:
Zoonotic Diseases Research Center, Ilam University of Medical Sciences, Ilam, Iran
Hassan Borji
Affiliation:
Faculty of Veterinary Medicine, Department of Pathobiology, Ferdowsi University of Mashhad, Mashhad, Iran
MohammadReza Chaechi Nosrati*
Affiliation:
Department of Pathobiology, Science and Research Branch, Islamic Azad University, Tehran, Iran
Ali Yousefi
Affiliation:
Students Research Center, Hamadan University of Medical Sciences, Hamadan, Iran
Morteza Shams
Affiliation:
Zoonotic Diseases Research Center, Ilam University of Medical Sciences, Ilam, Iran
*
Author for correspondence: Hamidreza Majidiani, MohammadReza Chaechi Nosrati, E-mail: Hamidreza.majidiani@gmail.com, h.majidiani@modres.ac.ir, mohammadchaichi1@gmail.com
Author for correspondence: Hamidreza Majidiani, MohammadReza Chaechi Nosrati, E-mail: Hamidreza.majidiani@gmail.com, h.majidiani@modres.ac.ir, mohammadchaichi1@gmail.com

Abstract

Current systematic review and meta-analysis demonstrate the prevalence reports of filariasis in animals in Iran along with human cases. Studies were screened, relevant papers were selected and the random-effect model was used by forest plot with 95% confidence interval (CI). Of 17 records of human case-reports, particularly from Khuzestan province (5 cases), Dirofilaria repens was the most detected parasite (10 cases) with higher involvement of the right eye (7 cases) than other organs. Eleven animal species were reported to be parasitised by filarioids in Iran. The prevalence of Dirofilaria immitis in canids was 14.69% (95% CI: 10.33–19.67), with highest rates (20.92%; 95% CI: 13.84–29.03) in free-ranging dogs. Male (10.07%; 95% CI: 5.10–16.47) and more than 1-year old (20.77%; 95% CI: 8.66–36.42) dogs were more likely to be found infected. The frequency of other filarioids of zoonotic interest was: Acanthocheilonema reconditum in dogs 2.15% (95% CI: 0.71–4.33), Dipetalonema evansi in camels 10.16% (95% CI: 4.73–17.34), Onchocerca cervicalis in horses 3.63% (95% CI: 1.44–6.75%) and Onchocerca fasciata 16.57% (95% CI: 10.12–24.24%) in camels. Still, our knowledge on parasitic filariae in Iran is limited and more investigation is needed in both human and animal populations.

Type
Review Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, R and Srivastava, AK (2007) Biochemical composition and metabolic pathways of filarial worms Setaria cervi: search for new antifilarial agents. Journal of Helminthology 81, 261280.CrossRefGoogle ScholarPubMed
Akhtardanesh, B, Radfar, MH, Voosough, D and Darijani, N (2011) Seroprevalence of canine heartworm disease in Kerman, southeastern Iran. Comparative Clinical Pathology 20, 573577.CrossRefGoogle Scholar
Alborzi, A, Mosallanejad, B, Najafabadi, M and Nikpoor, Z (2010) Infestation of heartworm (Dirofilaria immitis) in a cat in Ahvaz City: a case report. Journal of Veterinary Research 65, 255271.Google Scholar
Alho, AM, Meireles, J, Schnyder, M, Cardoso, L, Belo, S, Deplazes, P and de Carvalho, LM (2018) Dirofilaria immitis and Angiostrongylus vasorum: the current situation of two major canine heartworms in Portugal. Veterinary Parasitology 252, 120126.CrossRefGoogle ScholarPubMed
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission. UK: Cabi.CrossRefGoogle Scholar
Angelou, A, Gelasakis, AI, Verde, N, Pantchev, N, Schaper, R, Chandrashekar, R and Papadopoulos, E (2019) Prevalence and risk factors for selected canine vector-borne diseases in Greece. Parasites & vectors 12, 283.CrossRefGoogle Scholar
Anvari, D, Saadati, D, Siyadatpanah, A and Gholami, S (2019) Prevalence of dirofilariasis in shepherd and stray dogs in Iranshahr, southeast of Iran. Journal of Parasitic Diseases 43, 319323.CrossRefGoogle ScholarPubMed
Ashrafi, K, Golchai, J and Geranmayeh, S (2010) Human subcutaneous dirofilariasis due to Dirofilaria (Nochtiella) repens: clinically suspected as cutaneous fascioliasis. Iranian Journal of Public Health 39, 105.Google ScholarPubMed
Athari, A (2003) Zoonotic subcutaneous dirofilariasis in Iran. Archives of Iranian Medicine 6, 6365.Google Scholar
Azari-Hamidian, S, Yaghoobi-Ershadi, M, Javadian, E, Abai, M, Mobedi, I, Linton, YM and Harbach, R (2009) Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Medical and Veterinary Entomology 23, 111121.CrossRefGoogle Scholar
Azari-Hamidian, S, Norouzi, B and Harbach, RE (2019) A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance. Acta Tropica 194, 106122.CrossRefGoogle ScholarPubMed
Barrett, AW and Little, SE (2016) Vector-Borne infections in tornado-displaced and owner-relinquished dogs in Oklahoma, USA. Vector Borne and Zoonotic Diseases 16, 428430.CrossRefGoogle ScholarPubMed
Bech-Nielsen, S, Bornstein, S, Christensson, D, Wallgren, TB, Zakrisson, G and Chirico, J (1982) Parafilaria bovicola (Tubangui 1934) in cattle: epizootiology-vector studies and experimental transmission of Parafilaria bovicola to cattle. American Journal of Veterinary Research 43, 948954.Google Scholar
Boonyapakorn, C, Srikitjakarn, L, Morakote, N and Hoerchner, F (2008) The epidemiology of Dirofilaria immitis infection in outpatient dogs at Chiang Mai University Small Animal Hospital, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 39, 3338.Google Scholar
Borgsteede, FHM, van Wuijckhuise, L, Peutz, J, Roumen, T and Kock, P (2009) Import of Parafilaria bovicola in the Netherlands. Veterinary Parasitology 161, 146149.CrossRefGoogle ScholarPubMed
Borthakur, SK, Deka, DK, Islam, S, Sarma, DK and Sarmah, PC (2015) Prevalence and molecular epidemiological data on Dirofilaria immitis in dogs from Northeastern States of India. TheScientificWorldJournal 2015, 265385265385.CrossRefGoogle ScholarPubMed
Chatterjee, S and Nutman, TB (2015) Filarial nematodes. In Jorgensen, JH, Pfaller, MA and Carroll, KCManual of Clinical Microbiology, 11th Edn, ASM Press (US): American Society of Microbiology, pp. 24612470.Google Scholar
Cirovic, D, Penezic, A, Pavlovic, I, Kulisic, Z, Cosic, N, Burazerovic, J and Maletic, V (2014) First records of Dirofilaria repens in wild canids from the region of Central Balkan. Acta Veterinaria Hungarica 62, 481488.CrossRefGoogle ScholarPubMed
Diakou, A, Soubasis, N, Chochlios, T, Oikonomidis, IL, Tselekis, D, Koutinas, C, Karaiosif, R, Psaralexi, E, Tsouloufi, TK and Brellou, G (2019) Canine and feline dirofilariosis in a highly enzootic area: first report of feline dirofilariosis in Greece. Parasitology Research 118, 677682.CrossRefGoogle Scholar
Egbe-Nwiyi, TNC, Paul, BT and Muhammed, YY (2016) Haemoparasites and haematological parameters of the one humped camel (Camelus Dromedarius) slaughtered in Maiduguri Abattoir, Nigeria. Global Journal of Medical Research: Veterinary Science and Veterinary Medicine 16, 7.Google Scholar
Egger, M, Smith, GD, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629634.CrossRefGoogle ScholarPubMed
El-Khabaz, KAS, Abdel-Hakeem, SS and Arfa, MI (2019) Protozoan and helminthes parasites endorsed by imported camels (camel dromedaries) to Egypt. Journal of Parasitic Diseases 43, 607615.CrossRefGoogle Scholar
Espinoza, E, Cordero, M, Muro, A, Lorente, F and Simón, F (1993) Anti-Dirofilaria immitis IgE: seroepidemiology and seasonal variation in an exposed human population. Tropical medicine and parasitology: official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) 44, 172176.Google Scholar
Faísca, P, Morales-Hojas, R, Alves, M, Gomes, J, Botelho, M, Melo, M and Xufre, A (2010) A case of canine ocular onchocercosis in Portugal. Veterinary Ophthalmology 13, 117121.CrossRefGoogle ScholarPubMed
Genchi, C and Kramer, LH (2019) The prevalence of Dirofilaria immitis and D. repens in the Old world. Veterinary Parasitology 280, 108995. doi: https://doi.org/10.1016/j.vetpar.2019.108995.CrossRefGoogle Scholar
Gortázar, C, Castillo, J, Lucientes, J, Blanco, J, Arriolabengoa, A and Calvete, C (1994) Factors affecting Dirofilaria immitis prevalence in red foxes in northeastern Spain. Journal of Wildlife Diseases 30, 545547.CrossRefGoogle ScholarPubMed
Grácio, AJS, Richter, J, Komnenou, AT and Grácio, MA (2015) Onchocerciasis caused by Onchocerca lupi: an emerging zoonotic infection. Systematic review. Parasitology Research 114, 24012413.CrossRefGoogle ScholarPubMed
Gungel, H, Kara, N, Pinarci, EY, Albayrak, S, Baylancicek, DO and Uysal, HK (2009). An uncommon case with intravitreal worm. Intravitreal Dirofilaria infection. British Journal of Ophthalmology, 93, 573574, 697.CrossRefGoogle ScholarPubMed
Hamidinia, D, Maraghi, S, Azimi, F, Ai, A and Shirian, S (2016) The role of climate on prevalence or eradication of vesical schistosomiasis in Khuzestan Province of Iran. Journal of Parasitic Diseases 40, 387389.CrossRefGoogle ScholarPubMed
Hermosilla, C, Hetzel, U, Bausch, M, Grübl, J and Bauer, C (2005) First autochthonous case of canine ocular onchocercosis in Germany. Veterinary Record-English Edition 156, 450451.CrossRefGoogle ScholarPubMed
Higgins, JP, Thompson, SG, Deeks, JJ and Altman, DG (2003) Measuring inconsistency in meta-analyses. BMJ 327, 557560.CrossRefGoogle ScholarPubMed
Hodžić, A, Hinney, B, König, S, Naucke, T, Duscher, G and Joachim, A (2018) A case of ocular infection with Onchocerca lupi in a dog from Germany. Transboundary and Emerging Diseases 65, e214e216.CrossRefGoogle Scholar
Hornok, S, Genchi, C, Bazzocchi, C, Fok, E and Farkas, R (2007) Prevalence of Setaria equina microfilaraemia in horses in Hungary. Veterinary Record 161, 814816.Google ScholarPubMed
Ionică, AM, Matei, IA, D'Amico, G, Ababii, J, Daskalaki, AA, Sándor, AD, Enache, DV, Gherman, CM and Mihalca, AD (2017) Filarioid infections in wild carnivores: a multispecies survey in Romania. Parasites & vectors 10, 332332.CrossRefGoogle ScholarPubMed
Jamshidi, A, Jamshidi, M, Mobedi, I and Khosroara, M (2008) Periocular dirofilariasis in a young woman: a case report. The Korean journal of parasitology 46, 265.CrossRefGoogle Scholar
Khedri, J, Radfar, MH, Borji, H, Azizzadeh, M and Akhtardanesh, B (2014) Canine Heartworm in Southeastern of Iran with review of disease distribution. Iranian journal of parasitology 9, 560.Google ScholarPubMed
Khodabakhsh, M, Malmasi, A, Mohebali, M, Zarei, Z, Kia, EB and Azarm, A (2016) Feline Dirofilariosis due to Dirofilaria immitis in Meshkin Shahr District, Northwestern Iran. Iranian journal of parasitology 11, 269273.Google ScholarPubMed
Köse, M and Erdoğan, M (2012) Serological screening of canine heartworm (Dirofilaria immitis) infections in Turkey. Berliner und Munchener Tierarztliche Wochenschrift 125, 503508.Google ScholarPubMed
Kotwa, JD, Jardine, CM, Berke, O, Pearl, DL, Mercer, NJ and Peregrine, AS (2019) Prevalence and distribution of Dirofilaria immitis infection in wild canids in southern Ontario. Veterinary Parasitology: Regional Studies and Reports 18, 100349.Google ScholarPubMed
Krämer, F, Schaper, R, Schunack, B, Połozowski, A, Piekarska, J, Szwedko, A, Jodies, R, Kowalska, D, Schüpbach, D and Pantchev, N (2014) Serological detection of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis antibodies and Dirofilaria immitis antigen in a countrywide survey in dogs in Poland. Parasitology Research 113, 32293239.CrossRefGoogle Scholar
Kwarteng, A, Ahuno, ST and Akoto, FO (2016) Killing filarial nematode parasites: role of treatment options and host immune response. Infectious Diseases of Poverty 5, 86.CrossRefGoogle ScholarPubMed
Labelle, AL, Daniels, JB, Dix, M and Labelle, P (2011) Onchocerca lupi causing ocular disease in two cats. Veterinary Ophthalmology 14, 105110.CrossRefGoogle ScholarPubMed
Lee, AC, Montgomery, SP, Theis, JH, Blagburn, BL and Eberhard, ML (2010) Public health issues concerning the widespread distribution of canine heartworm disease. Trends in Parasitology 26, 168173.CrossRefGoogle ScholarPubMed
Little, SE, Beall, MJ, Bowman, DD, Chandrashekar, R and Stamaris, J (2014) Canine infection with Dirofilaria immitis, Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in the United States, 2010–2012. Parasites & Vectors 7, 257.CrossRefGoogle ScholarPubMed
Liu, C, Yang, N, He, J, Yang, M and Sun, M (2013) Prevalence of Dirofilaria immitis in dogs in Shenyang, Northeastern China. Korean Journal of Parasitology 51, 375377.CrossRefGoogle ScholarPubMed
Mahran, OM (2004) Some studies on blood parasites in camels (Camelus dromedarius) at Shalatin City, Red Sea Governorate. Assiut Veterinary Medical Journal 50, 172184.Google Scholar
Maia, C, Annoscia, G, Latrofa, MS, Pereira, A, Giannelli, A, Pedroso, L and Otranto, D (2015) Onchocerca lupi nematode in cat, Portugal. Emerging Infectious Diseases 21, 2252.CrossRefGoogle ScholarPubMed
Maraghi, S, Rahdar, M, Akbari, H, Radmanesh, M and Saberi, A (2006) Human dirofilariasis due to Dirofilaria repens in Ahvaz-Iran: a report of three cases. Pakistan Journal of Medical Sciences 22, 211213.Google Scholar
Maraghi, S, Sameri, A and Jeddi, Y (2015) Human Dirofilaria repens infection of the breast: a case report. Archives of Medical Laboratory Sciences 1, 4244. doi: https://doi.org/10.22037/amls.v1i1.9403.Google Scholar
Maraghi, S, Naini-Kashani, M, Masroupour, M, Sameri, A and Jeddi, Y (2016) Ophtalmic dirofilariasis. Archives of Medical Laboratory Sciences 2, 3638.Google Scholar
Marconcini, A, Magi, M, Macchioni, G and Sassetti, M (1996) Filariosis in foxes in Italy. Veterinary Research Communications 20, 316319.CrossRefGoogle ScholarPubMed
Marks, CA and Bloomfield, TE (1998) Canine heartworm (Dirofilaria immitis) detected in red foxes (Vulpes vulpes) in urban Melbourne. Veterinary Parasitology 78, 147154.CrossRefGoogle Scholar
Mirahmadi, H, Maleki, A, Hasanzadeh, R, Ahoo, MB, Mobedi, I and Rostami, A (2017) Ocular dirofilariasis by Dirofilaria immitis in a child in Iran: a case report and review of the literature. Parasitology International 66, 978981.CrossRefGoogle Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of Internal Medicine 151, 264269.CrossRefGoogle ScholarPubMed
Montoya-Alonso, JA, Mellado, I, Carretón, E, Cabrera-Pedrero, ED, Morchón, R and Simón, F (2010) Canine dirofilariosis caused by Dirofilaria immitis is a risk factor for the human population on the island of Gran Canaria, Canary Islands, Spain. Parasitology Research 107, 12651269.CrossRefGoogle ScholarPubMed
Mowlavi, G, Farzbod, F, Kheirkhah, A, Mobedi, I, Bowman, D and Naddaf, S (2014) Human ocular onchocerciasis caused by Onchocerca lupi (Spirurida. Onchocercidae) in Iran. Journal of Helminthology 88, 250255.CrossRefGoogle ScholarPubMed
Muhammad, G and Athar, M (2000) Dipetalonemiasis, Toxoplasmosis and piroplasmosis in camels. In Gahlot, TK (ed.), Selected Topics in Camelids. Chandan: Camel Publishing House, pp. 271274.Google Scholar
Mukendi, JP, Kimbita, E, Mbanzulu, KM, Maindo, PP and Misinzo, G (2016) Morphological and molecular detection of canine dirofilarial species of veterinary and medical importance in Morogoro municipality, Tanzania. Veterinary Parasitology 220, 13.CrossRefGoogle ScholarPubMed
Nabie, R, Spotin, A and Rouhani, S (2017) Subconjunctival setariasis due to Setaria equina infection; a case report and a literature review. Parasitology International 66, 930932.CrossRefGoogle ScholarPubMed
Negahban, S, Daneshbod, Y, Atefi, S, Daneshbod, K, Sadjjadi, SM, Hosseini, SV, Bedayat, GR and Abidi, H (2007) Dirofilaria repens diagnosed by the presence of microfilariae in fine needle aspirates. Acta Cytologica 51, 567570.CrossRefGoogle ScholarPubMed
Orihel, TC and Eberhard, ML (1998) Zoonotic filariasis. Clinical Microbiology Reviews 11, 366381.CrossRefGoogle ScholarPubMed
Oryan, A, Valinezhad, A and Bahrami, S (2008) Prevalence and pathology of camel filariasis in Iran. Parasitology Research 103, 11251131.CrossRefGoogle ScholarPubMed
Otranto, D and Deplazes, P (2019) Zoonotic nematodes of wild carnivores. International Journal for Parasitology: Parasites and Wildlife 9, 370383.Google ScholarPubMed
Otranto, D and Eberhard, ML (2011) Zoonotic helminths affecting the human eye. Parasites & vectors 4, 41.CrossRefGoogle ScholarPubMed
Otranto, D, Diniz, DG, Dantas-Torres, F, Casiraghi, M, de Almeida, IN, de Almeida, LN, dos Santos, JN, Furtado, AP, de Almeida Sobrinho, EF and Bain, O (2011a) Human intraocular filariasis caused by Dirofilaria sp. nematode, Brazil. Emerging Infectious Diseases 17, 863.CrossRefGoogle Scholar
Otranto, D, Sakru, N, Testini, G, Gürlü, VP, Yakar, K, Lia, RP, Dantas-Torres, F and Bain, O (2011b) First evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). The American journal of tropical medicine and hygiene 84, 5558.CrossRefGoogle Scholar
Otranto, D, Dantas-Torres, F, Cebeci, Z, Yeniad, B, Buyukbabani, N, Boral, OB, Gustinelli, A, Mounir, T, Mutafchiev, Y and Bain, O (2012) Human ocular filariasis: further evidence on the zoonotic role of Onchocerca lupi. Parasites & vectors 5, 84.CrossRefGoogle ScholarPubMed
Otranto, D, Dantas-Torres, F, Brianti, E, Traversa, D, Petrić, D, Genchi, C and Capelli, G (2013) Vector-borne helminths of dogs and humans in Europe. Parasites & vectors 6, 16.CrossRefGoogle ScholarPubMed
Otranto, D, Cantacessi, C, Dantas-Torres, F, Brianti, E, Pfeffer, M, Genchi, C, Guberti, V, Capelli, G and Deplazes, P (2015 a) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Veterinary Parasitology 213, 2437.CrossRefGoogle ScholarPubMed
Otranto, D, Giannelli, A, Latrofa, MS, Dantas-Torres, F, Trumble, NS, Chavkin, M, Kennard, G, Eberhard, ML and Bowman, DD (2015 b) Canine infections with Onchocerca lupi nematodes, United States, 2011–2014. Emerging Infectious Diseases 21, 868.CrossRefGoogle Scholar
Pampiglione, S and Rivasi, F (2000) Human dirofilariasis due to Dirofilaria (Nochtiella) repens: an update of world literature from 1995 to 2000. Dirofilaria 37, 82.Google Scholar
Panaitescu, D, Preda, A, Bain, O and Vasile-Bugarin, A (1999) Four cases of human filariosis due to Setaria labiatopapillosa found in Bucharest, Romania. Roumanian Archives of Microbiology and Immunology 58, 203207.Google ScholarPubMed
Pathak, KML and Chahabra, MB (2010) Parasites and parasitic diseases of the camel in India: a review. Indian Journal of Animal Sciences 80, 699706.Google Scholar
Pedram, N, Tabrizi, AS, Hosseinzadeh, S, Pourmontaseri, M and Rakhshandehroo, E (2019) Prevalence of Dirofilaria immitis and Dirofilaria repens in outdoor dogs in Tehran Province, Iran. Comparative Clinical Pathology 28, 15.CrossRefGoogle Scholar
Penezic, A, Selakovic, S, Pavlovic, I and Cirovic, D (2014) First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitology Research 113, 32813285.CrossRefGoogle ScholarPubMed
Radwan, AM, Ahmed, NE, Elakabawy, LM, Ramadan, MY and Elmadawy, RS (2016) Prevalence and pathogenesis of some filarial nematodes infecting donkeys in Egypt. Veterinary world 9, 888892.CrossRefGoogle ScholarPubMed
Reifur, L, Thomaz-Soccol, V and Montiani-Ferreira, F (2004) Epidemiological aspects of filariosis in dogs on the coast of Parana state, Brazil: with emphasis on Dirofilaria immitis. Veterinary Parasitology 122, 273286.CrossRefGoogle ScholarPubMed
Rjeibi, MR, Rouatbi, M, Mabrouk, M, Tabib, I, Rekik, M and Gharbi, M (2017) Molecular study of Dirofilaria immitis and Dirofilaria repens in dogs from Tunisia. Transboundary and Emerging Diseases 64, 15051509.CrossRefGoogle ScholarPubMed
Rodonaja, T (1967) A new species of Nematode, Onchocerca lupi n. sp., from Canis lupus cubanensis. Soobshchenyia Akad. Nauk Gruzinskoy SSR 45, 715719.Google Scholar
Rouhani, S and Athari, A (2003) Ocular dirofilariasis in Iran: a case report. Medical Journal of The Islamic Republic of Iran (MJIRI 17, 8586.Google Scholar
Saari, S, Nareaho, A and Nikander, S (2019) Canine Parasites and Parasitic Diseases. London, UK: Academic Press.Google Scholar
Sadighian, A (1969) Helminth parasites of stray dogs and jackals in Shahsavar area, caspian region, Iran. Journal of Parasitology 55, 372374.CrossRefGoogle ScholarPubMed
Salahi-Moghadam, A and Banihashemi, H (2016) Unusual location of dirofilaria immitis in A 5-year-old boy's hydrocele: a case report. Hormozgan Medical Journal 20, 210213.Google Scholar
Sazmand, A and Joachim, A (2017) Parasitic diseases of camels in Iran (1931–2017) – a literature review. Parasite 24, 21.CrossRefGoogle ScholarPubMed
Sazmand, A, Tafti, MH, Hekmatimoghaddam, S and Moobedi, I (2013) Dipetalonema evansi infection in camels of Iran's central area. Pakistan Journal of Biological Sciences 16, 647650.CrossRefGoogle ScholarPubMed
Sazmand, A, Eigner, B, Mirzaei, M, Hekmatimoghaddam, S, Harl, J, Duscher, GG, Fuehrer, H-P and Joachim, A (2016) Molecular identification and phylogenetic analysis of Dipetalonema evansi (LEWIS, 1882) in camels (Camelus dromedarius) of Iran. Parasitology Research 115, 16051610.CrossRefGoogle ScholarPubMed
Schwan, EV and Durand, DT (2002) Canine filariosis caused by Dirofilaria immitis in Mozambique: a small survey based on the identification of microfilariae. Journal of the South African Veterinary Association 73, 124126.CrossRefGoogle ScholarPubMed
Simon, F, Muro, A, Cordero, M and Martin, J (1991) A seroepidemiologic survey of human dirofilariosis in Western Spain. Tropical Medicine and Parasitology 42, 106108.Google ScholarPubMed
Simón, F, Siles-Lucas, M, Morchón, R, González-Miguel, J, Mellado, I, Carretón, E and Montoya-Alonso, JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clinical Microbiology Reviews 25, 507544.CrossRefGoogle ScholarPubMed
Simón, F, González-Miguel, J, Diosdado, A, Gómez, PJ, Morchón, R and Kartashev, V (2017) The complexity of zoonotic filariasis episystem and its consequences: a multidisciplinary view. BioMed Research International 2017, 10.CrossRefGoogle ScholarPubMed
Simsek, S, Utuk, AE, Koroglu, E and Rishniw, M (2008) Serological and molecular studies on Dirofilaria immitis in dogs from Turkey. Journal of Helminthology 82, 181186.CrossRefGoogle ScholarPubMed
Solgi, R, Sadjjadi, SM, Mohebali, M, Zarei, Z, Golkar, M and Raz, A (2018) Development of New recombinant DgK antigen for diagnosis of Dirofilaria immitis infections in dogs using ELISA technique and Its comparison to molecular methods. Iranian Biomedical Journal 22, 283.Google ScholarPubMed
Solismaa, M, Laaksonen, S, Nylund, M, Pitkanen, E, Airakorpi, R and Oksanen, A (2008) Filarioid nematodes in cattle, sheep and horses in Finland. Acta Veterinaria Scandinavica 50, 20.CrossRefGoogle ScholarPubMed
Stringfellow, GJ, Francis, IC, Coroneo, MT and Walker, J (2002) Orbital dirofilariasis. Clinical & Experimental Ophthalmology 30, 378380.CrossRefGoogle ScholarPubMed
Tabatabaei, SA, Soleimani, M, Nikmanesh, B, Mahmoudzadeh, R, Vahedian, Z, Salabati, M, Soleimani, Z, Matini, A and Noorbakhsh, M (2017) Human subconjunctival dirofilariasis presenting as the daytime photophobia: a case report. Iranian Journal of Public Health 46, 1430.Google ScholarPubMed
Tahir, D, Damene, H, Davoust, B and Parola, P (2017) First molecular detection of Dirofilaria immitis (Spirurida: Onchocercidae) infection in dogs from Northern Algeria. Comparative Immunology, Microbiology and Infectious Diseases 51, 6668.CrossRefGoogle ScholarPubMed
Ţălu, S, Ştefănuţ, A, Mihalca, A and Coroiu, Z (2012) Subconjunctival infestation with Setaria. Helminthologia 49, 119121.CrossRefGoogle Scholar
Tasić-Otašević, SA, Gabrielli, SV, Tasić, AV, MiladinovićTasić, NL, Kostić, JT, Ignjatović, AM, Dragonjić, LDP, Milošević, ZG, Arsić-Arsenijević, VS and Cancrini, GA (2014) Seroreactivity to Dirofilaria antigens in people from different areas of Serbia. BMC Infectious Diseases 14, 68.CrossRefGoogle ScholarPubMed
Tavakolizadeh, S and Mobedi, I (2009) Orbital dirofilariasis in Iran: a case report. The Korean journal of parasitology 47, 397.CrossRefGoogle ScholarPubMed
Taylor, , Hoerauf, A and Bockarie, M (2010) Lymphatic filariasis and onchocerciasis. The Lancet, 376, 11751185.CrossRefGoogle ScholarPubMed
Tekle, AH, Zouré, HG, Noma, M, Boussinesq, M, Coffeng, LE, Stolk, WA and Remme, JH (2016) Progress towards onchocerciasis elimination in the participating countries of the African Programme for Onchocerciasis Control: epidemiological evaluation results. Infectious Diseases of Poverty 5, 66.CrossRefGoogle ScholarPubMed
Theis, J (2005) Public health aspects of dirofilariasis in the United States. Veterinary Parasitology 133, 157180.CrossRefGoogle ScholarPubMed
Thompson, R, Lymbery, A and Smith, A (2010) Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 11631170.CrossRefGoogle ScholarPubMed
Tudor, P, Turcitu, M, Mateescu, C, Dantas-Torres, F, Tudor, N, Bărbuceanu, F, Ciuca, L, Burcoveanu, I, Acatrinei, D and Rinaldi, L (2016) Zoonotic ocular onchocercosis caused by Onchocerca lupi in dogs in Romania. Parasitology Research 115, 859862.CrossRefGoogle ScholarPubMed
Vieira, C, Vélez, I, Montoya, M, Agudelo, S, Alvarez, M, Genchi, C and Simon, F (1998) Dirofilaria immitis in Tikuna Indians and their dogs in the Colombian Amazon. Annals of Tropical Medicine and Parasitology 92, 123125.CrossRefGoogle ScholarPubMed
WHO (2015) Global programme to eliminate lymphatic filariasis: progress report, 2014. Weekly Epidemiological Record = Relevé épidémiologique hebdomadaire 90, 489504.Google Scholar
Zarei, Z, Kia, EB, Heidari, Z, Mikaeili, F, Mohebali, M and Sharifdini, M (2016) Age and sex distribution of Dirofilaria immitis among dogs in Meshkin-Shahr, northwest Iran and molecular analysis of the isolates based on COX1 gene. Veterinary Research Forum 7, 329334.Google ScholarPubMed
Supplementary material: File

Ghasemi et al. supplementary material

Ghasemi et al. supplementary material
Download Ghasemi et al. supplementary material(File)
File 428.3 KB