BACKGROUND: 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. METHODS: 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. RESULTS: 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. CONCLUSIONS: 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.

3rd Faculty of Medicine Charles University Prague Czech Republic

Wildlife Rehabilitation and Research Center of Ria Formosa Ria Formosa Natural Park Olhão Portugal

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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;63:802–807. doi: 10.1016/j.parint.2014.07.012. PubMed DOI

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. doi: 10.1017/S0022149X00019660. DOI

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;88:567–569. doi: 10.1590/S0074-02761993000400012. DOI

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;62:390–396. doi: 10.1016/j.parint.2013.04.001. PubMed DOI

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. PubMed

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;67:253–261. doi: 10.1016/j.parint.2017.12.007. PubMed DOI

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;79:101–103. doi: 10.4102/jsava.v79i2.254. PubMed DOI

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. doi: 10.1016/j.vetpar.2006.06.025. PubMed DOI

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;155:235–241. doi: 10.1016/j.vetpar.2008.05.004. PubMed DOI

Rolfe PF, Boray JC. Comparative efficacy of moxidectin, an ivermectin/clorsulon combination and closantel against immature paramphistomes in cattle. Aust Vet J. 1993;70:265–266. doi: 10.1111/j.1751-0813.1993.tb08047.x. PubMed DOI

Islam A. Comparative efficacy of ivermectin plus clorsulon and nitroxynil against naturally infected cattle. Eurasian J Vet Sci. 2013;29:43–45.

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;25:923–927. doi: 10.1016/0020-7519(95)00026-X. PubMed DOI

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;148:1458–1466. doi: 10.1017/S0031182021001153. PubMed DOI PMC

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;189:227–232. doi: 10.1016/j.vetpar.2012.04.019. PubMed DOI

Schuster RK. Philophthalmus aweerensis n sp. (Trematoda: Philophthalmidae) found in a rhea (Rhea americana) in the United Arab Emirates. Parasitol Res. 2011;109:1029–1033. doi: 10.1007/s00436-011-2340-5. PubMed DOI

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. doi: 10.1093/ofid/ofz265. PubMed DOI PMC

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. doi: 10.3390/pharmaceutics13070952. PubMed DOI PMC

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. doi: 10.1111/j.1463-5224.2012.01008.x. PubMed DOI

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;256:24–28. doi: 10.1016/j.vetpar.2018.04.011. PubMed DOI

Greve JH, Harrison GJ. Conjunctivitis caused by the eye flukes in captive-reared ostriches. J Am Vet Med Assoc. 1980;177:909–910. PubMed

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;49:983–985. PubMed

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;60:665–668. PubMed

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. doi: 10.1016/j.vetpar.2004.12.020. PubMed DOI

Gaudana R, Ananthula HK, Parenky A, Mitra AK. Ocular drug delivery. AAPS J. 2010;12:348–360. doi: 10.1208/s12248-010-9183-3. PubMed DOI PMC

Yadav M, Guzman-Aranguez A, de Perez MJ, Singh M, Singh J, Kaur IP. Bimatoprost loaded nanovesicular long-acting sub-conjunctival in-situ gelling implan vitro and in vivo evaluation. Materials Sci Eng C. 2019;103:109730. doi: 10.1016/j.msec.2019.05.015. PubMed DOI

Urtti A, Salminen L, Minalainen O. Systemic absorption of ocular pilocarpine is modified by polymer matrices. Int J Pharm. 1985;23:147–161. doi: 10.1016/0378-5173(85)90005-5. DOI

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;34:501–505. PubMed

Cruthers LR, Al-Khateeb GH, Hansen MF. Efficacy of levamisole (Tramisol) in drinking water against some nematodes of chickens. Proc Oklahoma Acad Sci. 1975;55:119–121.

El-Kholy H, Kemppainen B, Ravis W, Hoerr F. Pharmacokinetics of levamisole in broiler breeder chickens. J Vet Pharmacol Ther. 2006;29:49–53. doi: 10.1111/j.1365-2885.2006.00710.x. PubMed DOI

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;57:134–185. doi: 10.1016/j.preteyeres.2016.12.001. PubMed DOI