Recent large-scale philophthalmosis outbreak in Portugal: inefficacy of common antihelminthic agents

Parasites and Vectors - Tập 15 - Trang 1-7 - 2022
Petr Heneberg1, María Casero2
1Third Faculty of Medicine, Charles University, Prague, Czech Republic
2Wildlife Rehabilitation and Research Center of Ria Formosa (RIAS), Olhão, Portugal

Tóm tắt

Parasitic conjunctivitis caused by Philophthalmus spp. is a common ophthalmic disease in birds, with localized outbreaks occurring worldwide. There is no consensus on treating this disease; mechanical removal is considered a standard recommendation, but is associated with disease relapses within days or weeks. From 2015 to 2020, we examined 4295 Larus michahellis and Larus fuscus gulls in southern Portugal for the presence of Philophthalmus spp. Due to the need to treat dozens of infected gulls in the rescue station, we tested three treatment regimens aimed at targeting Philophthalmus lucipetus in the infected gulls: (I) the ophthalmic application of levamisole; (II) the oral application of milbemycin in combination with praziquantel; and (III) the subcutaneous application of ivermectin. The outbreak of philophthalmosis in gulls in southern Portugal has been ongoing since the first cases were reported in 2015–2016. The prevalence of philophthalmosis has fluctuated annually, peaking a maximum of 10.3% in L. fuscus in 2017 and at 2.1% in L. michahellis in 2016. The infection intensity peaked at a median of 11.5 eye-flukes per host bird in L. fuscus in 2016 and a median of six eye-flukes per host bird in L. michahellis in 2017. Nine gulls were infected with >50 eye-flukes. None of the treatment options were effective at treating P. lucipetus infections: the numbers of eye-flukes in the infected birds did not decrease, and the clinical signs of the disease did not change. An outbreak of philophthalmosis in southern Portugal has massively affected two species of gulls in the region. Two previously suggested philophthalmosis treatments (ocular levamisole and praziquantel given orally), as well as a third mode of treatment with a previously failed compound (ivermectin administered subcutaneously) were used. However, the treatments did not affect the numbers of P. lucipetus in the eyes of the treated gulls. Further research should address ophthalmic gel formulations or sub-conjunctival delivery mode for antihelminthic drugs that are effective against Philophthalmus spp. in vitro.

Tài liệu tham khảo

Gibson DI, Bray RA, Harris E. Host-parasite database of the Natural History Museum, London. London: Natural History Museum; 2005. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/index.html. Accessed 2 Dec 2021. Heneberg P, Rojas A, Bizos J, Kocková L, Malá M, Rojas D. Focal Philophthalmus gralli infection possibly persists in Melanoides tuberculata over two years following the definitive hosts’ removal. Parasitol Int. 2014;63:802–7. Pemberton R. Helminth parasites of three species of British gulls, Larus argentatus Pont., L. fuscus L. and L. ridibundus L. J Helminthol. 1963;37:57–88. Muniz-Pereira LC, Amato SB. Philophthalmus gralli (Digenea: Philophthalmidae) parasite of Anas bahamensis and Amazonetta brasiliensis, from Lagoons of Maricá county ,Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 1993;88:567–9. Literák I, Heneberg P, Sitko J, Wetzel EJ, Cardenas Callirgos JM, Čapek M, et al. Eye trematode infection in small passerines in Peru caused by Philophthalmus lucipetus, an agent with a zoonotic potential spread by an invasive freshwater snail. Parasitol Int. 2013;62:390–6. de Assis JCA, Pulido-Murillo E, de Melo AL, da Silva Martins NR, Pinto HA. Philophthalmus gralli in domestic waterfowl: an environmental study in an urban area from Brazil. Vet Parasitol Reg Stud Rep. 2022;29:100701. Heneberg P, Casero M, Waap H, Sitko J, Azevedo F, Těšínský M, et al. An outbreak of philophthalmosis in Larus michahellis and Larus fuscus gulls in Iberian Peninsula. Parasitol Int. 2018;67:253–61. Mukaratirwa S, Chimbwanda M, Matekwe N, Matenga E. A comparison of the efficacy of doramectin, closantel and levamisole in the treatment of the “oriental eye fluke”, Philophthalmus gralli, in commercially reared ostriches (Struthio camelus). J S Afr Vet Assoc. 2008;79:101–3. Hanna REB, Cromie L, Taylor SM, Couper A. The effect of a parenteral ivermectin/closantel injection on the growth and reproductive development of early immature Fasciola hepatica in cattle. Vet Parasitol. 2006;142:78–90. Borgsteede FHM, Taylor SM, Gaasenbeek CPH, Couper A, Cromie L. The efficacy of an ivermectin/closantel injection against experimentally induced infections and field infections with gastrointestinal nematodes and liver fluke in cattle. Vet Parasitol. 2008;155:235–41. Rolfe PF, Boray JC. Comparative efficacy of moxidectin, an ivermectin/clorsulon combination and closantel against immature paramphistomes in cattle. Aust Vet J. 1993;70:265–6. Islam A. Comparative efficacy of ivermectin plus clorsulon and nitroxynil against naturally infected cattle. Eurasian J Vet Sci. 2013;29:43–5. Shoop WL, Ostling DA, Rohrer SP, Mickle G, Haines HW, Michael BF, et al. Avermectins and milbemycins against Fasciola hepatica: in vivo drug efficacy and in vitro receptor binding. Int J Parasitol. 1995;25:923–7. Ico-Gómez R, González-Garduño R, Ortiz-Pérez D, Mosqueda-Gualito JJ, Flores-Santiago EDJ, Sosa-Pérez G, et al. Assessment of anthelminthic effectiveness to control Fasciola hepatica and paramphistome mixed infection in cattle in the humid tropics of Mexico. Parasitology. 2021;148:1458–66. Geurden T, Bartram D, Van Brussel L, Bo L, Scott-Baird E, Rugg D. Evaluation of the comparative efficacy of a moxidectin plus triclabendazole pour-on solution against adult and immature liver fluke, Fasciola hepatica, in cattle. Vet Parasitol. 2012;189:227–32. Schuster RK. Philophthalmus aweerensis n. sp. (Trematoda: Philophthalmidae) found in a rhea (Rhea americana) in the United Arab Emirates. Parasitol Res. 2011;109:1029–33. Sapp SGH, Alhabshan RN, Bishop HS, Fox M, Ndubuisi M, Snider CE, et al. Ocular trematodiasis caused by the avian eye fluke Philophthalmus in Southern Texas. Open Forum Infect Dis. 2019;6:ofz265. Prompetch T, Chailorm A, Tiwananthagorn S, Buranapim N, Okonogi S, Kato H, et al. Preclinical evaluations of modified rice hydrogel for topical ophthalmic drug delivery of praziquantel on avian philophalmiasis. Pharmaceutics. 2021;13:952. Church ML, Barrett PM, Swenson J, Kinsella JM, Tkach VV. Outbreak of Philophthalmus gralli in four greater rheas (Rhea americana). Vet Ophthalmol. 2013;16:65–72. Assis JCA, Martins NRS, Pinto HA. Experimental avian philophthalmosis: Evaluation of diagnosis and treatment of chickens infected with Philophthalmus gralli (Trematoda: Philophthalmidae). Vet Parasitol. 2018;256:24–8. Greve JH, Harrison GJ. Conjunctivitis caused by the eye flukes in captive-reared ostriches. J Am Vet Med Assoc. 1980;177:909–10. Martin CL. Ophthalmic disease in veterinary medicine. Boca Raton: CRC Press; 2009. Lyons ET, Drudge JH, Tolliver SC. Verification of ineffectual activity of ivermectin against adult Onchocerca spp in the ligamentum nuchae of horses. Am J Vet Res. 1988;49:983–5. Marley SE, Illyes EF, Keller DS, Meinert TR, Logan NB, Hendrickx MO, et al. Efficacy of topically administered doramectin against eyeworms, lungworms, and gastrointestinal nematodes of cattle. Am J Vet Res. 1999;60:665–8. Bianciardi P, Otranto D. Treatment of dog thelaziosis caused by Thelazia callipaeda (Spirurida, Thelaziidae) using a topical formulation of imidacloprid 10% and moxidectin 2.5%. Vet Parasitol. 2005;129:89–93. Gaudana R, Ananthula HK, Parenky A, Mitra AK. Ocular drug delivery. AAPS J. 2010;12:348–60. Yadav M, Guzman-Aranguez A, de Perez MJ, Singh M, Singh J, Kaur IP. Bimatoprost loaded nanovesicular long-acting sub-conjunctival in-situ gelling implant: In vitro and in vivo evaluation. Materials Sci Eng C. 2019;103:109730. Urtti A, Salminen L, Minalainen O. Systemic absorption of ocular pilocarpine is modified by polymer matrices. Int J Pharm. 1985;23:147–61. Pankavich JA, Poeschel GP, Shor AL, Gallo A. Evaluation of levamisole against experimental infections of Ascaridia, Heterakis, and Capillaria spp. in chickens. Am J Vet Res. 1973;34:501–5. Cruthers LR, Al-Khateeb GH, Hansen MF. Efficacy of levamisole (Tramisol) in drinking water against some nematodes of chickens. Proc Oklahoma Acad Sci. 1975;55:119–21. El-Kholy H, Kemppainen B, Ravis W, Hoerr F. Pharmacokinetics of levamisole in broiler breeder chickens. J Vet Pharmacol Ther. 2006;29:49–53. del Amo EM, Rimpelä A-K, Keikkinen E, Kari OK, Ramsay E, Lajunen T, et al. Pharmacokinetic aspects of retinal drug delivery. Prog Retin Eye Res. 2017;57:134–85.