Abstract
Oestrus ovis is the most common cause of human ophthalmomyiasis. So far, majority of ophthalmomyiasis cases have been reported from Mediterranean countries, but not from Croatia. In current study, we present first two cases of human ophthalmomyiasis in Croatia, caused by O. ovis larvae. Reviewing a PubMed database, additional 259 cases of human ophthalmomyiasis in countries of Mediterranean basin have been reported. A total of 260 (99.62%) cases had external, while 1 (0.38%) had internal form of ocular myiasis. In all cases, O. ovis larvae were identified as the causative agent. O. ovis infestation is usually reported in shepherds and farmers although there is a high prevalence of infection in urban areas as well. Various climatic factors influence O. ovis larvipositional activity. Air temperature is the most important factor affecting O. ovis larviposition, while humidity, wind speed, and time of the day play only a moderate role. Most common symptoms of ophthalmomyiasis are irritation and redness, and in more than half of cases infestation is multiple. Ophthalmomyiasis interna is eye-compromising condition. Since there is reduced awareness among patients and medical professionals, the real number of ophthalmomyiasis cases is probably significantly higher than published. Global warming predisposes future increase of O. ovis prevalence in humans, which emphasizes the need for mandatory reporting and surveillance of disease.
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References
Abdellatif MZ, Elmazar HM, Essa AB (2011) Oestrus ovis as a cause of red eye in Aljabal Algharbi, Libya. Middle East Afr J Ophthalmol 18(4):305–308. https://doi.org/10.4103/0974-9233.90133
Ahaduzzaman M (2019) The global and regional prevalence of oestrosis in sheep and goats: a systematic review of articles and meta-analysis. Parasit Vectors 12(1):346. https://doi.org/10.1186/s13071-019-3597-2
Akcakaya AA, Sargin F, Aslan ZI, Sevimli N, Sadigov F (2014) External ophthalmomyiasis seen in a patient from Istanbul, Turkey. Turkiye Parazitol Derg 38(3):205–207. https://doi.org/10.5152/tpd.2014.3512
Akdemir MO, Ozen S (2013) External ophthalmomyiasis caused by Oestrus ovis misdiagnosed as bacterial conjunctivitis. Trop Dr 43(3):120–123. https://doi.org/10.1177/0049475513492153
Alcaide M, Reina D, Frontera E, Navarrete I (2005a) Epidemiology of Oestrus ovis (Linneo, 1761) infestation in goats in Spain. Vet Parasitol 130(3–4):277–284. https://doi.org/10.1016/j.vetpar.2005.03.022
Alcaide M, Reina D, Sanchez-Lopez J, Frontera E, Navarrete I (2005b) Seroprevalence of Oestrus ovis (Diptera, Oestridae) infestation and associated risk factors in ovine livestock from southwestern Spain. J Med Entomol 42(3):327–331. https://doi.org/10.1093/jmedent/42.3.327
Anane S, Hssine LB (2010) Conjonctival human myiasis by Oestrus ovis in southern Tunisia. Bull Soc Pathol Exot 103(5):299–304. https://doi.org/10.1007/s13149-010-0081-9
Anderson JR, Nilssen AC (1996) Trapping oestrid parasites of reindeer: the response of Cephenemyia trompe and Hypoderma tarandi to baited traps. Med Vet Entomol 10(4):337–346
Angulo-Valadez CE, Ascencio F, Jacquiet P, Dorchies P, Cepeda-Palacios R (2011) Sheep and goat immune responses to nose bot infestation: a review. Med Vet Entomol 25(2):117–125. https://doi.org/10.1111/j.1365-2915.2010.00911.x
Arslan F, Mete B, Ozturk R, Samasti M (2010) External ophthalmomyiasis caused by Oestrus ovis in Istanbul. Trop Dr 40(3):186–187. https://doi.org/10.1258/td.2010.090464
Basmaciyan L, Gabrielle PH, Valot S, Sautour M, Buisson JC, Creuzot-Garcher C, Dalle F (2018) Oestrus ovis external ophtalmomyiasis: a case report in Burgundy France. BMC Ophthalmol 18(1):335. https://doi.org/10.1186/s12886-018-1003-z
Berrozpe-Villabona C, Avalos-Franco N, Aguilar-Munoa S, Baneros-Rojas P, Castellar-Cerpa J, Diaz-Valle D (2015) External ophthalmomyiasis. A case report from Spain. J Fr Ophtalmol 38(9):e219–e220. https://doi.org/10.1016/j.jfo.2015.03.014
Billi B, Lesnoni G, Audisio P, Giuliano MA, Rossi T, Costi E, Stirpe M (1997) Pars plana vitrectomy for retinal detachment due to internal posterior ophthalmomyiasis after cataract extraction. Graefes Arch Clin Exp Ophthalmol 235(4):255–258
Bonzon L, Toga I, Piarroux M, Piarroux R (2015) Clustered cases of Oestrus ovis ophthalmomyiasis after 3-week festival, Marseille, France, 2013. Emerg Infect Dis 21(2):375–377. https://doi.org/10.3201/eid2102.140974
Caliskan S, Ugurbas SC, Sagdik M (2014) Ophthalmomyiasis externa: three cases caused by Oestrus ovis larvae in Turkey. Trop Dr 44(4):230–232. https://doi.org/10.1177/0049475514531129
Carrillo I, Zarratea L, Suarez MJ, Izquierdo C, Garde A, Bengoa A (2013) External ophthalmomyiasis: a case series. Int Ophthalmol 33(2):167–169. https://doi.org/10.1007/s10792-012-9644-z
Cepeda-Palacios R, Scholl PJ (2000) Factors affecting the larvipositional activity of Oestrus ovis gravid females (Diptera: oestridae). Vet Parasitol 91(1–2):93–105
Dar MS, Amer MB, Dar FK, Papazotos V (1980) Ophthalmomyiasis caused by the sheep nasal bot, Oestrus ovis (Oestridae) larvae, in the Benghazi area of eastern Libya. Trans R Soc Trop Med Hyg 74(3):303–306. https://doi.org/10.1016/0035-9203(80)90087-5
Dokur M, Eroglu F, Ipek DN, Ulutasdemir N (2015) Two different myiasis cases in southeast of Turkey: ophthalmomyiasis and cutaneous myiasis. Parasitol Res 114(7):2767–2770. https://doi.org/10.1007/s00436-015-4455-6
Dono M, Bertonati MR, Poggi R, Teneggi E, Maddalo F, Via F, Orlandi R, Maroli M, Roncella S, Fedeli F, Battolla E (2005) Three cases of ophthalmomyiasis externa by sheep botfly Oestrus ovis in Italy. New Microbiol 28(4):365–368
Eyigor H, Dost T, Dayanir V, Basak S, Eren H (2008) A case of naso-ophthalmic myiasis. Kulak Burun Bogaz Ihtis Derg 18(6):371–373
Fathy FM, El-Barghathi A, El-Ahwal A, El-Bagar S (2006) Study on human ophthalmomyiasis externa caused by Oestrus ovis larva, in Sirte-Libya: parasite features, clinical presentation and management. J Egypt Soc Parasitol 36(1):265–282 following 282
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Francesconi F, Lupi O (2012) Myiasis. Clin Microbiol Rev 25(1):79–105. https://doi.org/10.1128/CMR.00010-11
Fries FN, Pattmöller M, Seitz B, Berger F, Kampen H, Szentmáry N, Becker SL (2018) Ophthalmomyiasis externa due to Oestrus ovis in a traveller returning from Greece. Travel Med Infect Dis 23:101–102. https://doi.org/10.1016/j.tmaid.2018.05.007
Sucilathangam G, Meenakshisundaram A, Hariramasubramanian S, Anandhi D, Palaniappan N, Anna T (2013a) External ophthalmomyiasis which was caused by sheep botfly (Oestrus ovis) larva: a report of 10 cases. J Clin Diagn Res 7(3):539–542. https://doi.org/10.7860/JCDR/2013/4749.2817
Glasgow BJ (1996) Ophthalmomyiasis. In: Pepose JS, Holland GN, Wilhelmus KR (eds) Occular infection and immunity. 1st edn. Mosby Publishers, St. Louis, pp 1505–1515
Gozum N, Kir N, Ovali T (2003) Internal ophthalmomyiasis presenting as endophthalmitis associated with an intraocular foreign body. Ophthalmic Surg Lasers Imaging 34(6):472–474
Grammer J, Erb C, Kamin G, Wild M, Riedinger C, Kosmidis P, Pleyer U, Thiel HJ (1995) Ophthalmomyiasis externa due to the sheep botfly Oestrus ovis (Diptera: Oestridae) in southwest Germany. Ger J Ophthalmol 4(3):188–195
Istek S (2014) Ophthalmomyiasis externa from Hakkari, the south east border of Turkey. BMJ Case Rep 2014. https://doi.org/10.1136/bcr-2013-201226
Jenzeri S, Ammari W, Attia S, Zaouali S, Babba H, Messaoud R, Khairallah M (2009) External ophthalmomyiasis manifesting with keratouveitis. Int Ophthalmol 29(6):533–535. https://doi.org/10.1007/s10792-008-9261-z
Kuk S, Yildirim S, Ozden M, Erensoy A, Saki CE (2009) Ophthalmomyiasis is not only a problem for rural regions of Eastern Anatolia of Turkey. Med Sci Monit 15(11):CS166–CS168
Macdonald PJ, Chan C, Dickson J, Jean-Louis F, Heath A (1999) Ophthalmomyiasis and nasal myiasis in New Zealand: a case series. N Z Med J 112(1100):445–447
Mazzeo V, Ercolani D, Trombetti D, Todeschini R, Gaiba G (1987) External ophthalmomyiasis. Report of four cases. Int Ophthalmol 11(2):73–76
Morsy TA, Farrag AM (1991) Two cases of human ophthalmomyiasis. J Egypt Soc Parasitol 21(3):853–855
Narayanan S, Jayaprakash K (1991) Incidence of ocular myiasis due to infection with the larva of oestrus ovis (Oestridae Diptera). Indian J Ophthalmol 39(4):176–178
Nicoli RM, Lanfranchi J, Jarry D (1962) Les myiases humaines a Oestridae (Oestrasis) (Diptera: Brachycera). Bull Soc Entomol 67:108–113
Ozyol P, Ozyol E, Sankur F (2016) External ophthalmomyiasis: a case series and review of ophthalmomyiasis in Turkey. Int Ophthalmol 36(6):887–891. https://doi.org/10.1007/s10792-016-0204-9
Pampiglione S (1957a) Ocular myiasis in humans in Italy; critical review of described cases. Nuovi Ann Ig Microbiol 8(4):410–421
Pampiglione S (1957b) Two further cases of ocular myiasis: anterior internal ophthalmomyiasis (fourth case in Italy) and conjunctival external ophthalmomyiasis. Nuovi Ann Ig Microbiol 8(1):59–69
Pampiglione S (1958a) Epidemiologic study of human conjunctival myiasis by Oestrus ovis in Italy. I. Survey among Italian doctors. Nuovi Ann Ig Microbiol 9(3):242–263
Pampiglione S (1958b) Epidemiological findings on human myiasis caused by Oestrus ovis in Italy. II. Survey on shepherds. Nuovi Ann Ig Microbiol 9(6):494–517
Pampiglione S, Giannetto S, Virga A (1997) Persistence of human myiasis by Oestrus ovis L. (Diptera: Oestridae) among shepherds of the Etnean area (Sicily) for over 150 years. Parassitologia 39(4):415–418
Panadero-Fontan R, Otranto D (2015) Arthropods affecting the human eye. Vet Parasitol 208(1–2):84–93. https://doi.org/10.1016/j.vetpar.2014.12.022
Parikh V, Biswas J, Vaijayanthi K, Das D, Raval V (2011) Bilateral ocular myiasis interna caused by botfly (Oestrus ovis): a case report. Ocul Immunol Inflamm 19(6):444–447. https://doi.org/10.3109/09273948.2011.622455
Parola P, Socolovschi C, Jeanjean L, Bitam I, Fournier PE, Sotto A, Labauge P, Raoult D (2008) Warmer weather linked to tick attack and emergence of severe rickettsioses. PLoS Negl Trop Dis 2(11):e338. https://doi.org/10.1371/journal.pntd.0000338
Perez Dieste JM, Castroviejo Bolibar M, Sanchez Servate C (2018) Ophthalmomyasis by Oestrus ovis. Arch Soc Esp Oftalmol 93(11):e75. https://doi.org/10.1016/j.oftal.2018.06.019
Priour DJ (1980) Ocular myiasis in a Texas sheep shearer. Tex Med 76(10):52–53
Punjabi OS, Browning DJ, Clark L, Antoszyk AN (2019) “Pacman” invasion of the retina: two cases of ophthalmomyiasis interna posterior. Am J Ophthalmol Case Rep 15:100491. https://doi.org/10.1016/j.ajoc.2019.100491
Reingold WJ, Robin JB, Leipa D, Kondra L, Schanzlin DJ, Smith RE (1984) Oestrus ovis ophthalmomyiasis externa. Am J Ophthalmol 97(1):7–10. https://doi.org/10.1016/0002-9394(84)90439-2
Rivasi F, Campi L, Cavallini GM, Pampiglione S (2009) External ophthalmomyiasis by Oestrus ovis larvae diagnosed in a Papanicolaou-stained conjunctival smear. Cytopathology 20(5):340–342. https://doi.org/10.1111/j.1365-2303.2008.00579.x
Sacca G, Gabrielli L, Stella E (1965) Notes on Oestrus ovis L. (Diptera, Oestridae) and description of some cases of myiasis in humans. Ann Ist Super Sanita 1(1):73–94
Sante Fernandez L, Hernandez-Porto M, Tinguaro V, Lecuona Fernandez M (2017) Ophthalmomyiasis and nasal myiasis by Oestrus ovis in a patient from the Canary Islands with uncommon epidemiological characteristics. Enferm Infecc Microbiol Clin 35(7):461–462. https://doi.org/10.1016/j.eimc.2015.10.003
Smillie I, Gubbi PK, Cocks HC (2010) Nasal and ophthalmomyiasis: case report. J Laryngol Otol 124(8):934–935. https://doi.org/10.1017/S0022215109992714
Sucilathangam G, Meenakshisundaram A, Hariramasubramanian S, Anandhi D, Palaniappan N, Anna T (2013b) External ophthalmomyiasis which was caused by sheep botfly (Oestrus ovis) larva: a report of 10 cases. J Clin Diagn Res 7(3):539–542. https://doi.org/10.7860/JCDR/2013/4749.2817
Sundu C, Dinc E, Kurtulus UC, Yildirim O (2015) Ophthalmomyiasis externa: a report of three cases. Turk J Ophthalmol 45(5):220–222. https://doi.org/10.4274/tjo.70456
Tabuenca-Del Barrio L, Mozo-Cuadrado M, Zubicoa-Eneriz A, Plaza-Ramos P (2018) Ocular external myiasis. A series of cases due to larvae Oestrus ovis in Navarra, Spain. Arch Soc Esp Oftalmol 93(11):567–570. https://doi.org/10.1016/j.oftal.2018.05.016
Taylor MA (2012) Emerging parasitic diseases of sheep. Vet Parasitol 189(1):2–7. https://doi.org/10.1016/j.vetpar.2012.03.027
Weinand FS, Bauer C (2001) Ophthalmomyiasis externa acquired in Germany: case report and review of the literature. Ophthalmologica 215(5):383–386. https://doi.org/10.1159/000050891
White GB (1996) Chapter 88. In: Cook CG, Zumla A (eds) Manson’s tropical diseases, 22nd edition. 22 edn. WB Sauders Publishers, London, pp 1526–1532
Winfield CR, Burgess NR (1983) Oestrus ovis ophthalmomyiasis in Cyprus. J R Army Med Corps 129(3):154–155
Wolfelschneider P, Wiedemann P (1996) External ophthalmic myiasis cause by Oestrus ovis (sheep and goat botfly). Klin Monatsbl Augenheilkd 209(4):256–258. https://doi.org/10.1055/s-2008-1035314
Zammarchi L, Giorni A, Gabrielli S, Strohmeyer M, Cancrini G, Bartoloni A (2014) Human oestriasis acquired in Florence and review on human myiasis in Italy. Parasitol Res 113(6):2379–2385. https://doi.org/10.1007/s00436-014-3906-9
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The authors would like to thank Mr. Robert Nezirović for assistance with interlibrary requests and database searches, and Mr. Boris Popović for help with graphic design.
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Pupić-Bakrač, A., Pupić-Bakrač, J., Škara Kolega, M. et al. Human ophthalmomyiasis caused by Oestrus ovis—first report from Croatia and review on cases from Mediterranean countries. Parasitol Res 119, 783–793 (2020). https://doi.org/10.1007/s00436-019-06599-x
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DOI: https://doi.org/10.1007/s00436-019-06599-x