Abstract
Globalization has increased circulation of people, their food, livestock and pets in the world, and changes in the environment, climate and human behaviour have led to the rapid expansion of emerging infections throughout the world. One of the reasons of a new pathogen affecting humans is the passage from an animal to a human being. Onchocerca (O.) lupi, a filarial worm first described in a wolf in 1967, is an emerging pathogen which has been incriminated as the etiological agent for 205 canine, 2 feline and 18 human infections in Europe, Tunisia, Turkey, Iran and the USA. Most frequent findings in animals and humans are monolateral or asymmetrical variably painful subconjunctival swellings and nodules containing immature or mature worms affecting the eye and/or adjacent tissues accompanied by conjunctival hyperemia. Occasionally, subcutaneous nodules and masses affecting the spinal cord have been observed in humans. Diagnosis of O. lupi is achieved by microscopy of excised adult female worms which exhibit a particular cuticular structure and molecular analysis. Treatment consists in worm removal accompanied by antihelminthic, antibiotic and anti-inflammatory therapy.
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References
Afonso-Roque MMA, Mendonça MM, Gil LI (1982) Inquérito a oncocercose e a outras filarioses em Portugal—Resultados preliminares. Port Ciênc Veter 77(461):33–39
Alexandre NM, Revez N, Gomes P, Baker J (2006) Um caso de episclerite nodular por Onchocerca sp. em cão. XIV Congresso Nacional da Associação Portuguesa de Médicos Veterinários Especialistas em Animais de Companhia; Estoril, Portugal 2006
Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission. CABI Publish, Wallingford, Oxon, UK
Azarova NS, Miretsky OY, Soniry MD (1965) The first instance of detection of Nematode Onchocerca Diesing 1841 in a person in the U.R.S.S. Med Parasit Parasit Dis Moscow 34:156–158
Bain O, Chabaud AG (1986) Atlas des larves infestantes de filaires. Trop Med Parasitol 37:301–340
Bandi C, Anderson TJC, Genchi C, Blaxter ML (1998) Phylogeny of Wolbachia in filarial nematodes. Proc Roy Soc London B 265:2407–2413
Bandi C, Trees AJ, Brattig NW (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 98:215–238
Bergua A, Hohberger B Held J Muntau B, Tannich E, Tappe D (2015) Human case of Onchocerca lupi infection, Germany, August 2014 Eurosurv 20(16) 23 04 2015 epub
Berry R, Stepenaske S, Dehority W, Almeida M, Nmathison B, Bishop H, Eberhard M (2014) Zoonotic Onchocerca lupi presenting as a subcutaneous nodule in a 10-year-old girl: report of the second case in the United states and a review of the literature. Abstract Book of ASDP annual meeting, Nov 6–9, 2014, Chicago, USA Oral presentations.
Bishop HS, Mathinson BA, Hoffman RS (2012) Short report: ocular zoonotic Onchocerca infection in a resident of Oregon. Am J Trop Med Hyg 87(6):1073–1075
Biswas A, Yassin MH (2013) An unsuspected cause of eye irritation: a case of zoonotic ocular onchocerciasis. Case Rep Infect Dis 2013:504749. doi:10.1155/2013/504749, Epub 2013 Dec 3
Blacklock DB (1926) The development of Onchocerca volvulus in Simulium damnosum. Ann Trop Med Parasitol 20:1–48
Bryant J (1935) Endemic retino-choroiditis in the Anglo-Egyptian Sudan and its possible relationship to Onchocerca volvulus. Trans Roy Soc Trop Med Hyg 28:523–532
Burr WE Jr, Brown MF, Eberhard ML (1998) Zoonotic Onchocerca (Nematoda: Filaroidea) in the cornea of a Colorado resident. Ophthalmology 105(8):1494–1497
Charalambous M, Shelley AJ, Grácio AJS, Raybould JN (1994) Cytogenetical analysis of the Simulium damnosum complex (Diptera: Simuliidae) in Guinea Bissau. Vet Entomol 9:34–42
Crosskey RW (1987) An annoted checklist of the world blackflies (Diptera: Simuliidae). In Blackflies, the Pennsylvania, State University 1987: 425–506.4 in Dalmat HT edt. The blackflies (Diptera: Simuliidae) of Guatemala and their role as vectors of onchocerciasis. Smithsonian Misc Coll 125:1–425
Crosskey R (1990) The natural history of blackflies. Wiley Ltd, U.K., pp 71–86
Davies L, Down AER, Weitz B, Williams CB (1962) Studies on blackflies (Diptera: Simuliidae) taken in a light trap in Scotland. II: blood meal identification by precipitin test. Trans R Ent Soc London 114:21–27
Dudley RW, Smith C, Dishop M, Mirsky D, Handler MH, Rao S (2015) A cervical spine mass caused by Onchocerca lupi. Lancet S0140-6736(14):62255–62258. doi:10.1016/S0140-6736(14)62255-8, Epub ahead of print
Eberhard ML, Ortega Y, Dial S, Schiler CA, Sears W, Greiner E (2000) Ocular Onchocerca infection in Western United States. Vet Parasitol 90:333–338
Eberhard M, Ostovar GA, Chundu K, Hobohm D, Feiz-Erfan I, Mathison BA, Bishop HS, Cantey PT (2013) Zoonotic Onchocerca lupi infection in a 22-month-old child in Arizona: first report in the United States and a review of the literature. Am J Trop Med Hyg 88:601–605
Eberhard ML, Sims AC, Bishop HS, Mathinson BA, Hoffman RS (2012) Short report: ocular zoonotic Onchocerca infection in a resident of Oregon. Am J Trop Med Hyg 87(6):1073–1075
Egyed Z, Sréter T, Széll Z, Beszteri B, Oravecz O, Marialigeti K, Varga I (2001) Morphologic and genetic characterization of Onchocerca lupi infecting dogs. Vet Parasitol 102(4):309–319
Egyed Z, Sréter T, Szél Z, Nyiro G, Márialigeti K, Varga L (2002) Molecular phylogeny analysis of Onchocerca lupi and its Wolbachia endosymbiont. Vet Parasitol 108(2):153–161
Faísca P, Morales-Hojas R, Alves M, Gomes J, Botelho M, Xufre A (2010) A case of canine ocular onchocerciasis in Portugal. Vet Ophthalmol 13:117–121
Franchini D, Giannelli A, Di Paola G, Corete H, Cardoso L, Lia RP, Campbell BE, Dantas-Torres LD, Assa EA, Ricciardi M, Valastro C, Cavaliere L, Di Belloi A, Otranto D (2014) Image diagnosis of zoonotic onchocerciasis by Onchocerca lupi. Vet Parasitol 203(1–2):91–95
Fuentes I, Montes I, Saugar JM, Latrofa S, Gárate T, Otranto D (2012) Thelaziosis in humans, a zoonotic infection, Spain, 2011. Emerg Infect Dis 18(12):2073–2075
Gardiner CH, Dick EJ Jr, Meininger AC, Lozano-Alarcon F, Jackson F (1993) Onchocerciasis in two dogs. J Am Vet Med Assoc 203:828–830
Giannelli A, Cantacessi C, Graves P, Becker L, Campbel BE, Dantas-Torres F, Otranto D (2014) A preliminary investigation of serological tools for the detection of Onchocerca lupi infection in dogs. Parasitol Res 113(5):1989–1991
Gionfriddo JR, Mangan B, Wilkerson G, Powell CC, Friedman DS, Ehrhart EJ (2005) A challenging case a dog with ocular masses. Vet Med 100:570–576
Grácio, AJS (1985a) Estudo sistemático e bioecológico dos Simulídeos de Portugal (Diptera: Simuliidae) PhD thesis; Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa: 238–242; 247–253; 270–276; 277–280; 299–303; 304–310; 314–318; 322–330; 331–344; 365–369; 493–496
Grácio AJS (1985b) The blackflies (Diptera: Simuliidae) of Portugal. Systematic and geographical distribution in Algarve (Southern Portugal). Rev Iber Parasitol 45(1):15–23
Grácio AJS (1991) Estudo dos simulídeos de Portugal (Diptera: Simuliidae): Nota prévia sobre o seu papel como vectores de filárias do género Onchocerca. I Cong. Int. Assoc. Subocidental Europea de Parasitologia 1991: 261
Grácio AJS, Grácio MA (2012) Study on animal onchocerciasis in Portugal: parasites and its vectors in Santarém and Portalegre districts. Acta Parasitol Port 19(1/2):176–177
Grácio AJS, Grácio MA (2013) Filariasis and blackflies (Diptera: Simuliidae) in Europe: Portugal. Trop Med and Int Health 18(suppl 1):1108–1231
Grácio AJS, Fadia A, Shelley AJ, Molyneux D (1995) Onchocerciasis in Guinea Bissau. European Commission, DG XII, Second Programme (1987–1991), Summaries of the final reports, A Parasitology: 571–574
Grácio AJS, Shelley AJ, Raybould JA, Forte JG, Lowry CA, Nhaque AT, Molyneux D, Grácio MA (2010) Eco-epidemiology of the onchocerciasis in Guinea Bissau (West Africa): a review. Acta Parasitol Port 17(1):23–39
Hermosilla A, Hetzel U, Bausch M, Grubl J, Bauer C (2002) First autochthonous case of canine ocular onchocerciasis in Germany. Vet Rec 108(2):153–161
Hise AG, Gillette-Ferguson I, Pearleman E (2004) The role of endosymbiotic Wolbachia bacteria in filarial disease. Cell Microbiol 6:97–104
Hissete J (1932) Memoire sur l’Onchocerca volvulus Leukart et ses manifestation oculaires au Congo Belge. Ann Soc Bélg Trop Parasitol Mycol 12:433–529
Hoerauf A, Volkmann L, Hamelmann C, Adjei O, Autenrieth B, Fleischer B, Büttner DW (2000) Endosymbiontic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 355(9211):1242–1243
Hoerauf A, Specht S, Marfo-Debrekyei Y, Büttner M, Yaw Debrah A, Mand S, Batsa L, Brattig N, Konadu P, Bandi C, Fimmers R, Adjei O, Büttner DW (2009) Efficacy of 5-week doxycycline treatment on adult Onchocerca volvulus. Parasitol Res 104:437–447
Ilhan HD, Yaman A, Morishima Y, Sugiyama H, Yamasaki MMH, Hasegawa H, Lebe B, Bajin MS (2013) Onchocerca lupi infection in Turkey: a unique case of a rare human parasite. Acta Parasitol 58(3):384–388
Kalogeropoulos CD, Stefaniotou MI, Gorgoli KE, Papadopoulou CV, Pappa CN, Paschidis CA (2014) Ocular dirofilariasis: a case series of 8 patients. Middle East Afr J Ophthalmol 21(4):312–316
Komnenou A, Koutinas AF (2007) Ocular manifestations of some canine infectious and parasitic diseases commonly encountered in the Mediterranean. Euro J Comp Anim Pract 17:271–279
Komnenou A, Eberhard M, Kaedrymidou E, Tsaile E, Dessiris A (2002) Subconjuctival filariasis due to Onchocerca sp. in dogs. Vet Ophthalmol 5:119–126
Komnenou A, Egyed Z, Sréter T, Eberhard ML (2003) Canine onchocercosis in Greece: report of further 20 cases and molecular characterization of the parasite and its Wolbachia endosymbiont. Vet Parasitol 118:151–155
Labelle AL, Daniels JB, Dix M, Labelle P (2011) Onchocerca lupi causing disease in two cats. Vet Ophthalmol 14(Suppl 1):105–110
Labelle AL, Maddox CW, Daniels JB, Lanka S, Eggett TE, Dubielzig RR, Labelle P (2013) Canine ocular onchocercosis in the United States is associated with Onchocerca lupi. Vet Parasitol 193:297–301
Landmann F, Voronin D, Sullivan W, Taylor MJ (2011) Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. PLoS Pathog 7(11):e1002351
Lok JB, Walker ED, Scoles GA (2000). Filariasis. In Medical Entomology. Kluwer Academic Publisher: 299–375
Maia C, Delgado E, Peleteiro C, Campino L (2011) Ocular clinical manifestations and histopathological features in experimental canine leishmaniasis. Acta Parasitol Port 18(1/2):37–44
Mendonça MM, Afonso-Roque (1982) Oncocercoses in Portugal—Resultats preliminaires. Rev Iberica Parasitol; Vol Extra:439–447
Milinovich GJ, Williams GM, Clements ACA, Hu W (2014) Internet-based surveillance systems for monitoring emerging infectious disease. Lancet Infect Dis 14(2):160–168
Mowlavi G, Farzbod F, Kheirkhah A, Mobedi I, Bowman DD, Naddaf SR (2013) Human ocular onchocerciasis caused by Onchocerca lupi (Spirurida, Onchocercidae) in Iran. J Helminthol 88(2):250–255
Muller R (1983) Species recognition in human filarioids. In: Stone A, Platt HM, Khalie IF (eds) Concepts in nematode systematics. Academic Press, London, pp 335–349
Mutafchiev Y, Dantas-Torres F, Gianelli A, Abramo l, Cortes H, Otranto D (2013) Redescription of Onchocerca lupi (Spirurida: Onchocercidae), with histopathological observations. Parasites & Vectors 6:309–316
Orihel TC, Ash LR, Holshuh HJ, Santenelli S (1991) Onchocerciasis in a Californian dog. Am J Trop Med Hyg 44:513–517
Otranto D, Testini G, Gurlu VP, Yakar K, Dantas-Torres F, Bain O (2011) First evidence human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg 84:55–58
Otranto D, Dantas-Torres F, Cebeci Z, Yeniad B, Buyukbabani N, Boal OB, Gustinelli A, Mounir T, Mutafchiev Y, Bain O (2012) Human ocular onchocersiasis further evidence zoonotic role of Onchocerca lupi. Parasites Vectors 5:84
Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Papadopoulos E, Cardoso L, Cortes H (2013a) Zoonotic Onchocerca lupi infection in dogs, Greece and Portugal, 2011–2012. Emerg Infect Dis 19(12):2000–2003
Otranto D, Dantas-Torres F, Gianneli A, Abramo F, Ignajatovic Cupina A, Petric D, Cardoso I, Mutafchiev Y, Cortes H (2013b) Cutaneous distribution and circadian rhythm of Onchocerca lupi microfilariae in dogs. Plos Neg Trop Dis 7(12):e 2585. doi:10.1371/Journal.pndt.0002585
Otranto D, Giannelli A, Scotty Trumble N, Chavkin M, Kennard G, Latrofa MS, Bowman DD, Dantas-Torres F, Eberhard ML (2015) Clinical case presentation and a review of the literature of canine onchocercosis by Onchocerca lupi in the United States. Parasit Vectors 8(1):699
Pampiglione S, Vakalis N, Lyssimachou A, Kouppari G, Orihel TC (2001) Subconjunctival zoonotic Onchocerca in an Albanian man. Ann Trop Med Parasitol 95:827–832
Ridley H (1945) Ocular onchocerciasis including an investigation in the Gold Coast. Brit J Ophthalmol 10(Suppl):1–58
Rishniw M, Barr SC, Simpson KW, Frongillo MF, Franz M, Dominguez Alpizar JL (2006) Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 135(3–4):303–314
Robles R (1917) Enfermidad nueva in Guatemala. Juven Med 17:97–115
Rodojana TE (1967) A new species of Nematode, Onchocerca lupi n. sp. from Canis lupus cubanensis. Soobshchenyia Akad Nauk Gruzinskoy, SSR45: 715–719
Sallo F, Eberhard ML, Fok E, Baska F, Hatvani I (2005) Zoonotic intravitreal Onchocerca in Hungary. Am Acad Ophthalmol 112:502–504
Schäffer EH, Marquart KH, Brandes K, Kunder S, Jennen (2006) Okuläre Onchozerkose bei einem Hund. Tierärztl Praxis 34:178–184
Shelley AJ (1991) Simuliidae and transmission and control of human onchocerciasis in Latin America. Cad Saude Publica RJ7(3):310–327
Simonsen PE, Fischer PU, Hoerauf A, Weil GJ (2013) The filariases. In: Farrar J, Hotez PJ, Junghanss T, Kang G, Lalloo D (eds) White eds. Manson’s tropical diseases, 23rd edn. Elsevier Saunders, Edinburgh, U.K, pp 737–765
Sironi M, Bandia C, Sacchi L, Di Sacco B, Dumiani G, Genchi C (1995) A close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol Biochem Parasitol 74:223–227
Specht S, Hoerauf A, Adjei O, Debrah A, Büttner DW (2009) Newly acquired Onchocerca volvulus filariae after doxycycline treatment. Parasitol Res 106:23–31
Sréter T, Széll Z (2008) Onchocerciasis a newly recognized disease in dogs. Vet Parasitol 153:1–13
Sréter T, Széll Z, Egyed Z, Varga I (2002) Subconjunctival zoonotic onchocerciasis in a man: aberrant infection with Onchocerca lupi? Ann Trop Med Parasitol 96:497–502
Sréter-Lancz Z, Széll Z, Sréter T (2007) Molecular genetic comparison of Onchocerca sp. dogs in Europe with other spirurid nematodes including Onchocerca lienalis. Vet Parasitol 148:365–370
Strong RP, Becquaert JC, Sandground JH, Munoz OM (1934) Onchocerciasis with special reference of the Central America form of the disease. Harward University Press, Cambridge, Massachusetts, pp 1–234
Széll Z, Erdélyi L, Sréter T, Albert M, Varga I (2001) Canine ocular onchocerciasis in Hungary. Vet Parasitol 97:243–249
Takaoka H, Fukuda M, Oisuka Y, Aoki C, Uni S, Bain O (2012) Blackflies vectors of zoonotic onchocerciasis in Japan. Med Vet Entomol 2(4):372–378
Taylor MJ, Hoerauf A (1999) Wolbachia bacteria of filarial nematodes. Parasitol Today 15(11):437–442
Vakalis NC, Himonas CA (1997) Human and canine dirofilariasis in Greece. Parassitologia 39(4):389–391
World Health Organization (2015) Prevention of blindness and visual impairment. Onchocerciasis Control Programme (OCP). www.who.int last accessed Apr 6, 2015
Zarfoss MK, Dubielzig RR, Eberhard ML, Schmidt KS (2005) Canine ocular onchocerciasis in the United States: two new cases and a review of the literature. Vet Ophthalmol 8(1):51–57
Ziadi S, Trimèche M, Mestiri S, Mokni M, Trabelsi A, Ben Abdelkader Ben Said M, Ben Hadj Hamida F, Korbi S (2005) La dirofilariose sous-conjonctivale humaine. A propos de deux cas tunisiens. J Fr Ophtalmol 28:e2
Zwick H, Werner D (1999) Simuliidae. In Entomofauna Germanica. 2. Checkliste der Dipteren Deutschlands. Eds H. Schumann, R. Bährmann, Stark. Studia Dipterologica 2 (Suppl), 80–82
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Grácio, A.J.S., Richter, J., Komnenou, A.T. et al. Onchocerciasis caused by Onchocerca lupi: an emerging zoonotic infection. Systematic review. Parasitol Res 114, 2401–2413 (2015). https://doi.org/10.1007/s00436-015-4535-7
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DOI: https://doi.org/10.1007/s00436-015-4535-7
Keywords
- Onchocerciasis
- Onchocerca spp
- Onchocerca lupi
- Zoonosis
- Ocular disease
- Ocular lesions
- Vectors
- Dogs
- Cats
- Simuliidae
- Blackflies
- Wolbachia sp