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Confirmed cases of human Onchocerca lupi infection: a systematic review of an emerging threat

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Abstract

Diverse Onchocerca species are present mostly parasitizing ungulates, with the exception of Onchocerca volvulus (O. volvulus) in humans and O. lupi in canids and cats. The human cases due to the O. lupi have been more highlighted during last years. So, the present review was performed to determine the detailed characteristics of confirmed human O. lupi case reports documented worldwide. Hence, a systematic search was done using English international databases (Scopus, PubMed, Web of Science, Embase, ProQuest, and Google Scholar). Totally, 14 confirmed human cases were documented during the last decade, mostly from the USA and Turkey with 7 and 3 cases, respectively. Most cases (7 individuals) were male with the age range of 22-month-old to 54-year-old. The parasite was frequently isolated from the right eye (5 cases), followed by the left eye (4 cases), cervical spinal canal (3 cases), scalp, and right forearm (one case each). Molecular identification of the isolated agent was the preferred way of diagnosis in most cases (9 records). In conclusion, human O. lupi cases have been more highlighted in recent years, whether due to the improved diagnostics and/or host-switching phenomenon, and both veterinarians and healthcare authorities should be alerted.

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References

  • Adler PH, McCreadie JW (2019) Black flies (Simuliidae) medical and veterinary entomology. Elsevier, p 237–259

  • Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission. Cabi

  • Azarova N, Miretsky O, Sonin M (1965) The first instance of detection of nematode Onchocerca Diesing, 1841 in a person in the USSR. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 34(2):156–158

    CAS  Google Scholar 

  • Bain O (1981) Le genre Onchocerca: hypothèses sur son évolution et clé dichotomique des espèces. Ann Parasitol Hum Comp 56(5):503–526

    Article  CAS  PubMed  Google Scholar 

  • Basáñez M-G, Pion SD, Boakes E, Filipe JA, Churcher TS, Boussinesq M (2008) Effect of single-dose ivermectin on Onchocerca volvulus: a systematic review and meta-analysis. Lancet Infect Dis 8(5):310–322

    Article  PubMed  Google Scholar 

  • Bergua A, Hohberger B, Held J, Muntau B, Tannich E, Tappe D (2015) Human case of Onchocerca lupi infection, Germany, august 2014. Eurosurveillance 20(16) https://doi.org/10.2807/1560-7917.ES2015.20.16.21099

  • Biswas A, Yassin MH (2013) An unexpected cause of eye irritation: a case of zoonotic ocular onchocerciasis. Case reports in infectious diseases 2013

  • Bosch F, Manzanell R, Mathis A (2016) First description of Onchocerca jakutensis (Nematoda: Filarioidea) in red deer (Cervus elaphus) in Switzerland. International Journal for Parasitology: Parasites and Wildlife 5(2):192–197

    PubMed  PubMed Central  Google Scholar 

  • Burr WE Jr, Brown MF, Eberhard ML (1998) Zoonotic Onchocerca (Nematoda: Filarioidea) in the cornea of a Colorado resident. Ophthalmology 105(8):1494–1497

    Article  PubMed  Google Scholar 

  • Cambra-Pellejà M, Gandasegui J, Balaña-Fouce R, Muñoz J, Martínez-Valladares M (2020) Zoonotic implications of Onchocerca species on human health. Pathogens 9(9):761

    Article  PubMed Central  CAS  Google Scholar 

  • Cantey PT et al (2016) The emergence of zoonotic Onchocerca lupi infection in the United States - a case-series. Clin Infect Dis 62(6):778–783. https://doi.org/10.1093/cid/civ983

    Article  PubMed  Google Scholar 

  • Carvalho Cabral P, Olivier M, Cermakian N (2019) The complex interplay of parasites, their hosts, and circadian clocks. Front Cell Infect Microbiol 9:425

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chabaud AG, Bain O (1994) The evolutionary expansion of the Spirurida. Int J Parasitol 24(8):1179–1201

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Moon K, deMello DE, Feiz-Erfan I, Theodore N, Bhardwaj RD (2015) Case report of an epidural cervical Onchocerca lupi infection in a 13-year-old boy. J Neursurg Pediatr 16(2):217–221

    Article  Google Scholar 

  • Colella V, Lia R, Di Paola G, Cortes H, Cardoso L, Otranto D (2018a) International dog travelling and risk for zoonotic Onchocerca lupi. Transboundary Emer Dis 65(4):1107–1109

    Article  CAS  Google Scholar 

  • Colella V et al. (2018b) Evaluation of oxfendazole in the treatment of zoonotic Onchocerca lupi infection in dogs. PLoS Negl Trop Dis 12(1):e0006218

  • Currie DC, Adler PH (2007) Global diversity of black flies (Diptera: Simuliidae) in freshwater Freshwater Animal Diversity Assessment. Springer, p 469–475

  • Dantas-Torres F, Otranto D (2020a) Overview on Dirofilaria immitis in the Americas, with notes on other filarial worms infecting dogs. Vet Parasitol 282:109113

  • Dantas-Torres F, Otranto D (2020b) Overview on Dirofilaria immitis in the Americas, with notes on other filarial worms infecting dogs. Vet Parasitol:109113

  • de Almeida M et al (2020) Duplex real-time PCR assay for clinical differentiation of Onchocerca lupi and Onchocerca volvulus. Am J Trop Med Hyg 103(4):1556–1562

    Article  PubMed  PubMed Central  Google Scholar 

  • Deplazes P, Eckert J, von Samson-Himmelstjerna G, Zahner H (2012) Lehrbuch der Parasitologie für die Tiermedizin. Georg Thieme Verlag

  • Dudley RW, Smith C, Dishop M, Mirsky D, Handler MH, Rao S (2015) A cervical spine mass caused by Onchocerca lupi. The Lancet 386(10001):1372

    Article  Google Scholar 

  • Eberhard ML, Sims AC, Bishop HS, Mathison BA, Hoffman RS (2012) Ocular zoonotic Onchocerca infection in a resident of Oregon. Am J Trop Med Hyg 87(6):1073–1075

    Article  PubMed  PubMed Central  Google Scholar 

  • Eberhard ML et al (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(3):601–605

    Article  PubMed  PubMed Central  Google Scholar 

  • Egyed Z et al (2001) Morphologic and genetic characterization of Onchocerca lupi infecting dogs. Vet Parasitol 102(4):309–319

    Article  CAS  PubMed  Google Scholar 

  • Egyed Z, Sréter T, Széll Z, Nyirő G, Márialigeti K, Varga I (2002) Molecular phylogenetic analysis of Onchocerca lupi and its Wolbachia endosymbiont. Vet Parasitol 108(2):153–161

    Article  CAS  PubMed  Google Scholar 

  • Ghasemi E et al (2020) Filarial worms: a systematic review and meta-analysis of diversity in animals from Iran with emphasis on human cases. Parasitology 147(9):909–921

    Article  PubMed  Google Scholar 

  • Grácio AJS, Richter J, Komnenou AT, Grácio MA (2015) Onchocerciasis caused by Onchocerca lupi: an emerging zoonotic infection. Systematic Review Parasitol Res 114(7):2401–2413

    Article  PubMed  Google Scholar 

  • Hassan HK et al (2015) Isolation of Onchocerca lupi in dogs and black flies, California, USA. Emerg Infect Dis 21(5):789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodžić A, Hinney B, König S, Naucke T, Duscher G, Joachim A (2018) A case of ocular infection with Onchocerca lupi in a dog from Germany. Transboundary Emer Dis 65(1):e214–e216

    Article  Google Scholar 

  • Hoerauf A et al (2008) Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med Microbiol Immunol 197(3):295–311

    Article  CAS  PubMed  Google Scholar 

  • Hussein H, El Mannan AA, El Sinnary K (1988) Onchocerca armillata Railliet and Henry, 1909 andOnchocerca gutturosa (Neumann, 1910) in camels (Camelus dromedarius L.) in the Sudan. Veterinary research communications 12(6):475–480

  • Ilhan H et al (2013a) Onchocerca lupi infection in Turkey: a unique case of a rare human parasite. Acta Parasitol 58(3):384–388

    Article  PubMed  Google Scholar 

  • Ilhan HD et al. (2013b) Onchocerca lupi infection in Turkey: a unique case of a rare human parasite. vol 58, p 384–388

  • Koehsler M, Soleiman A, Aspöck H, Auer H, Walochnik J (2007) Onchocerca jakutensis filariasis in humans. Emerg Infect Dis 13(11):1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labelle AL, Daniels JB, Dix M, Labelle P (2011) Onchocerca lupi causing ocular disease in two cats. Vet Ophthalmol 14:105–110

    Article  PubMed  Google Scholar 

  • Latrofa MS, et al. (2018) A real-time PCR tool for the surveillance of zoonotic Onchocerca lupi in dogs, cats and potential vectors. PLoS Negl Trop Dis 12(4):e0006402

  • Ma G et al (2018) Human toxocariasis. Lancet Infect Dis 18(1):e14–e24

    Article  PubMed  Google Scholar 

  • Maia C et al (2015) Onchocerca lupi nematode in cat. Portugal Emerg Infect Dis 21(12):2252

    Article  PubMed  Google Scholar 

  • Miró G et al (2016) First detection of Onchocerca lupi infection in dogs in southern Spain. Parasit Vectors 9(1):1–3

    Article  CAS  Google Scholar 

  • Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341

    Article  PubMed  Google Scholar 

  • Mowlavi G, Farzbod F, Kheirkhah A, Mobedi I, Bowman DD, Naddaf SR (2014) Human ocular onchocerciasis caused by Onchocerca lupi (Spirurida, Onchocercidae) in Iran. J Helminthol 88(2):250–255. https://doi.org/10.1017/S0022149X13000060

    Article  CAS  PubMed  Google Scholar 

  • Mutafchiev Y et al (2013) Redescription of Onchocerca lupi (Spirurida: Onchocercidae) with histopathological observations. Parasit Vectors 6(1):309

    Article  PubMed  PubMed Central  Google Scholar 

  • Orihel TC, Eberhard ML (1998) Zoonotic filariasis. Clin Microbiol Rev 11(2):366–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otranto D, Deplazes P (2019) Zoonotic nematodes of wild carnivores. International Journal for Parasitology: Parasites and Wildlife 9:370–383

    PubMed  PubMed Central  Google Scholar 

  • Otranto D et al (2011) First evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg 84(1):55–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D et al (2012b) Human ocular filariasis: further evidence on the zoonotic role of Onchocerca lupi. Parasit Vectors 5(1):84

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D, Dantas-Torres F, Papadopoulos E, Petrić D, Ćupina AI, Bain O (2012c) Tracking the vector of Onchocerca lupi in a rural area of Greece. Emerg Infect Dis 18(7):1196

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D et al (2013a) Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 6(1):1–14

    Article  Google Scholar 

  • Otranto D et al (2015) Canine infections with Onchocerca lupi nematodes, United States, 2011–2014. Emerg Infect Dis 21(5):868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otranto D et al (2012a) Human ocular filariasis: further evidence on the zoonotic role of Onchocerca lupi. Parasit Vectors 5(1). https://doi.org/10.1186/1756-3305-5-84

  • Otranto D et al (2013b) Cutaneous distribution and circadian rhythm of Onchocerca lupi microfilariae in dogs. PLoS Negl Trop Dis 7(12):e2585

  • Otranto D et al (2013c) Zoonotic Onchocerca lupi infection in dogs, Greece and Portugal, 2011–2012. Emerg Infect Dis 19(12):2000

  • Pampiglione S, Vakalis N, Lyssimachou A, Kouppari G, Orihel T (2001) Subconjunctival zoonotic Onchocerca in an Albanian man. Ann Trop Med Parasitol 95(8):827–832

    Article  CAS  PubMed  Google Scholar 

  • Rodonaja T (1967) A new species of Nematode, Onchocerca lupi n. sp., from Canis lupus cubanensis. Soobshchenyia Akad Nauk Gruzinskoy SSR 45:715–719

    Google Scholar 

  • Roe CC et al (2020) Coyotes as reservoirs for Onchocerca lupi, United States, 2015–2018. Emerg Infect Dis 26(12):2989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sallo F, Eberhard ML, Fok E, Baska F, Hatvani I (2005) Zoonotic intravitreal onchocerca in Hungary. Ophthalmology 112(3):502–504

    Article  PubMed  Google Scholar 

  • Sandell T, Skogen AR, Lier T, Pettersen FO (2020) Human ocular Onchocerca lupi infection diagnosed in Norway. International Journal of Travel Medicine and Global Health 8(4):170–173

    Article  Google Scholar 

  • Simonsen PE, Fischer PU, Hoerauf A, Weil GJ (2013) The filariases manson’s tropical diseases: Twenty-Third Edition. Elsevier Ltd, p 737–765

  • Sréter T, Széll Z (2008) Onchocercosis: a newly recognized disease in dogs. Vet Parasitol 151(1):1–13

    Article  PubMed  Google Scholar 

  • Takaoka H et al (1996) Second case of zoonotic Onchocerca infection in a resident of Oita in Japan. Parasite 3(2):179–182

    Article  CAS  PubMed  Google Scholar 

  • Takaoka H et al (2005) An Onchocerca species of wild boar found in the subcutaneous nodule of a resident of Oita. Japan Parasitol Int 54(1):91–93

    Article  PubMed  Google Scholar 

  • Uni S et al (2010) Zoonotic filariasis caused by Onchocerca dewittei japonica in a resident of Hiroshima Prefecture, Honshu. Japan Parasitol Int 59(3):477–480

    Article  PubMed  Google Scholar 

  • Uni S et al (2015) New zoonotic cases of Onchocerca dewittei japonica (Nematoda: Onchocercidae) in Honshu. Japan Parasites & Vectors 8(1):1–10

    CAS  Google Scholar 

  • Vakalis N, Himonas C (1997) Human and canine dirofilariasis in Greece. Parassitologia 39(4):389–391

    CAS  PubMed  Google Scholar 

  • Verocai GG et al (2016) Onchocerca lupi nematodes in dogs exported from the United States into Canada. Emerg Infect Dis 22(8):1477

    Article  PubMed  PubMed Central  Google Scholar 

  • Verocai GG, Nelson KJ, Callahan RT, Wekesa JW, Hassan HK, Hoberg EP (2018) A cryptic species of Onchocerca (Nematoda: Onchocercidae) in blackflies (Simulium spp.) from southern California, USA. Parasites & vectors 11(1):1–11

  • Wesołowska M et al (2020) Onchocerca jakutensis ocular infection in Poland: a new vector-borne human health risk? Parasit Vectors 13(1):1–4

    Article  Google Scholar 

  • WHO (2014) Onchocerciasis. World Health Organization, Regional Office for the Eastern Mediterranean

    Google Scholar 

  • Ziadi S et al. (2005) La dirofilariose sous-conjonctivale humaine: à propos de deux cas tunisiens. Journal Français d'Ophtalmologie 28(7):773. e1–773. e4

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Correspondence to Morteza Shams or Hamidreza Majidiani.

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Asghari, A., Adhami, G., Shariatzadeh, S.A. et al. Confirmed cases of human Onchocerca lupi infection: a systematic review of an emerging threat. Parasitol Res 120, 3633–3644 (2021). https://doi.org/10.1007/s00436-021-07309-2

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