Cutaneous myiasis in cats and dogs: Cases, predisposing conditions and risk factors
Corresponding Author
Marco Pezzi
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Correspondence
Marco Pezzi, Department of Life Sciences and Biotechnology, University of Ferrara, Via L. Borsari 46, 44121 Ferrara, Italy.
Email: [email protected]
Contribution: Conceptualization, Data curation, Investigation, Methodology, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorChiara Scapoli
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorMilvia Chicca
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Validation, Writing - original draft, Writing - review & editing
Search for more papers by this authorMarilena Leis
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Funding acquisition, Writing - original draft, Writing - review & editing
Search for more papers by this authorMaria Gabriella Marchetti
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorCarlo Nicola Francesco Del Zingaro
Veterinary Clinic, Alfonsine Ravenna, Italy
Contribution: Investigation, Methodology, Writing - original draft
Search for more papers by this authorChiara Beatrice Vicentini
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Investigation, Writing - original draft
Search for more papers by this authorElisabetta Mamolini
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft
Search for more papers by this authorAnnunziata Giangaspero
Department of the Sciences of Agriculture, Food and Environment, University of Foggia, Foggia, Italy
Contribution: Investigation, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorTeresa Bonacci
Department of Biology, Ecology and Earth Science, University of Calabria, Arcavacata di Rende, Cosenza, Italy
Contribution: Investigation, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Marco Pezzi
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Correspondence
Marco Pezzi, Department of Life Sciences and Biotechnology, University of Ferrara, Via L. Borsari 46, 44121 Ferrara, Italy.
Email: [email protected]
Contribution: Conceptualization, Data curation, Investigation, Methodology, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorChiara Scapoli
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorMilvia Chicca
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Validation, Writing - original draft, Writing - review & editing
Search for more papers by this authorMarilena Leis
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Funding acquisition, Writing - original draft, Writing - review & editing
Search for more papers by this authorMaria Gabriella Marchetti
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorCarlo Nicola Francesco Del Zingaro
Veterinary Clinic, Alfonsine Ravenna, Italy
Contribution: Investigation, Methodology, Writing - original draft
Search for more papers by this authorChiara Beatrice Vicentini
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Investigation, Writing - original draft
Search for more papers by this authorElisabetta Mamolini
Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Contribution: Supervision, Writing - original draft
Search for more papers by this authorAnnunziata Giangaspero
Department of the Sciences of Agriculture, Food and Environment, University of Foggia, Foggia, Italy
Contribution: Investigation, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorTeresa Bonacci
Department of Biology, Ecology and Earth Science, University of Calabria, Arcavacata di Rende, Cosenza, Italy
Contribution: Investigation, Supervision, Writing - original draft, Writing - review & editing
Search for more papers by this authorFunding information
Funding for this study was provided by “Consorzio Futuro in Ricerca” (Ferrara, Italy), code n. COFELEIS42/18, assigned to Marilena Leis.
Abstract
Two cases of cutaneous myiasis diagnosed in 2018 in Emilia-Romagna region (northern Italy) were reported. The first one, described in a domestic cat Felis silvestris catus L. (Carnivora: Felidae) and caused by Calliphora vicina Robineau-Desvoidy (Diptera: Calliphoridae), was the first one of this type ever reported in Italy in cats. The second one was described in a domestic dog Canis lupus familiaris L. (Carnivora: Canidae) and caused by Lucilia sericata (Meigen) (Diptera: Calliphoridae) and was unusual because it occurred in absence of lesions. An extensive literature search on cutaneous myiasis in these two domestic animal species was performed in order to draw attention to predisposing conditions and risk factors.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
REFERENCES
- Azeredo-Espin, A. M., & Madeira, N. G. (1996). Primary myiasis in dog caused by Phaenicia eximia (Diptera: Calliphoridae) and preliminary mitochondrial DNA analysis of the species in Brazil. Journal of Medical Entomology, 33, 839–843. https://doi.org/10.1093/jmedent/33.5.839
- Bonacci, T., & Brandmayr, P. (2016). Primi dati sui ditteri che causano miasi canine in Calabria. Proceedings of the 25th National Italian Congress of Entomology. June 20 to 24, Padua, Italy. p. 315
- Bonacci, T., Curia, G., Leoncini, R., & Whitmore, D. (2017). Traumatic myiasis in farmed animals caused by Wohlfahrtia magnifica in southern Italy (Diptera: Sarcophagidae). Fragmenta Entomologica, 49, 57–60. https://doi.org/10.4081/fe.2017.230
10.4081/fe.2017.230 Google Scholar
- Bonacci, T., Greco, S., Whitmore, D. & Curcio, U. (2013). First data on myiasis caused by Wohlfahrtia magnifica (Schiner, 1862) (Insecta: Diptera: Sarcophagidae) in Calabria, southern Italy. Life: the Excitement of Biology, 1, 197–201. https://doi.org/10.9784/LEB1(4)Bonacci.02
10.9784/LEB1(4)Bonacci.02 Google Scholar
- Cansi, E. R., & Demo, C. (2011). Ocorrência de miíases em animais de companhia no Distrito Federal, Brasil. Acta Scientiae Veterinariae, 39, 1–5.
- Carnevali, F., Franchini, D., Otranto, D., Giangaspero, A., Di Bello, A., Ciccarelli, S., Szpila, K., Valastro, C., & van der Esch, A. S. (2019). A formulation of neem and hypericum oily extract for the treatment of the wound myiasis by Wohlfahrtia magnifica in domestic animals. Parasitology Research, 118, 2361–2367. https://doi.org/10.1007/s00436-019-06375-x
- Chemonges-Nielsen, S. (2003). Chrysomya bezziana in pet dogs in Hong Kong: A potential threat to Australia. Australian Veterinary Journal, 81, 202–205. https://doi.org/10.1111/j.1751-0813.2003.tb11471.x
- Choe, S., Lee, D., Park, H., Jeon, H. K., Kim, H., Kang, J. H., Jee, C. H., & Eom, K. S. (2016). Canine wound myiasis caused by Lucilia sericata (Diptera: Calliphoridae) in Korea. Korean Journal of Parasitology, 54, 667–671. https://doi.org/10.3347/kjp.2016.54.5.667
- Choi, J., Kim, H., Na, J., Kim, S. H., & Park, C. (2015). Cutaneous myiasis associated with tick infestations in a dog. Journal of Veterinary Clinics, 32, 473–475. https://doi.org/10.17555/jvc.2015.10.32.5.473
10.17555/jvc.2015.10.32.5.473 Google Scholar
- Cramer-Ribeiro, B. C., Sanavria, A., Monteiro, H. H. M. S., de Oliveira, M. Q., & de Souza, F. S. (2003). Inquiry of cases of myiasis by Dermatobia hominis in dogs (Canis familiaris) of the Northern and Western zone of Rio de Janeiro city in 2000. Brazilian Journal of Veterinary Research and Animal Science, 40, 21–28.
10.1590/S1413-95962003000100002 Google Scholar
- de Souza, C. P., Verocai, G. G., & Ramadinha, R. H. (2010). Myiasis caused by the New World screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae) in cats from Brazil: Report of five cases. Journal of Feline Medicine and Surgery, 12, 166–168. https://doi.org/10.1016/j.jfms.2009.08.003
- Dik, B., İlhan, C., Ceylan, O., & Uzunlu, E. O. (2018). The first case of traumatic myiasis caused by Musca domestica in a dog in Konya, Turkey. Turkish Journal of Veterinary and Animal Sciences, 42, 1–4. https://doi.org/10.3906/vet-1803-65
- Dik, B., Uslu, U., & Işik, N. (2012). Myiasis in animals and human beings in Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 18, 37–42. https://doi.org/10.9775/kvfd.2011.4654
- Eren, H., Aypak, S., Ural, K., & Seven, F. (2010). Traumatic myiasis in a dog and ocular myiasis in a cat cases due to Lucilia sericata (Diptera: Calliphoridae) larvaes. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16, 883–886. https://doi.org/10.9775/kvfd.2010.1844
- Farkas, R., Hall, M. J., Bouzagou, A. K., Lhor, Y., & Khallaayoune, K. (2009). Traumatic myiasis in dogs caused by Wohlfahrtia magnifica and its importance in the epidemiology of wohlfahrtiosis of livestock. Medical and Veterinary Entomology, 23(Suppl 1), 80–85.
- Fois, F., Mereu, P. P., Cappai, S., Vanin, S., Maistrello, L., Deiana, A. M., Cabras, P. A., & Liciardi, M. (2012). Myiasis by Wohlfahrtia magnifica (Diptera: Sarcophagidae) in different mammals in Sardinia. Proceedings of the 27th National Congress of Italian Society of Parasitology. June 26 to 29; Alghero, Italy. p. 107.
- Francesconi, F., & Lupi, O. (2012). Myiasis. Clinical Microbiology Reviews, 25, 79–105. https://doi.org/10.1128/CMR.00010-11
- Gatt, P., & Zammit, T. (2008). First record of Oestrus ovis Linnaeus, 1758 from Malta, and case reports of myiasis from the Maltese Islands (Diptera: Brachycera). Bulletin of the Entomological Society of Malta, 1, 5–10.
- Gökpinar, S., & Karsli, B. (2018). Traumatic myiasis associated with Wohlfahrtia magnifica and Lucilia sericata larvae in dog. Van Veterinary Journal, 29, 55–57.
- Hall, M. J. R., & Farkas, R. (2000). Traumatic myiasis of humans and animals. In L. B. Papp, & B. Darvas (Eds.), Contributions to a manual of Palaearctic Diptera, Volume 1. General and applied dipterology (pp. 751–768). Science Herald.
- Hall, M. J. R., & Smith, K. G. C. (1993). Diptera causing myiasis in man. In R. P. Lane, & R. W. Crosskey (Eds.), Medical insects and arachnids (pp. 429–469). Chapman and Hall.
10.1007/978-94-011-1554-4_12 Google Scholar
- Hall, M. J., Wall, R. L., & Stevens, J. R. (2016). Traumatic myiasis: A neglected disease in a changing world. Annual Review of Entomology, 61, 159–716. https://doi.org/10.1146/annurev-ento-010715-023655
- Han, H. S., Toh, P. Y., Yoong, H. B., Loh, H. M., Tan, L. L., & Ng, Y. Y. (2018). Canine and feline cutaneous screw-worm myiasis in Malaysia: Clinical aspects in 76 cases. Veterinary Dermatology, 29, 442-e148. https://doi.org/10.1111/vde.12672
- Hinaidy, H. K., & Frey, H. (1984). Weitere Fakultativmyiasis-Fälle bei Wirbeltieren in Osterreich. Wiener Tierärztliche Monatsschrift, 71, 237–238.
- Işık, N., & Dik, B. (2015). Bir köpekte Lucilia sericata (Diptera: Calliphoridae)’dan kaynaklanan travmatik myiasis olgusu. Eurasian Journal of Veterinary Sciences, 31, 242–244.
10.15312/EurasianJVetSci.2015413530 Google Scholar
- Johnson, S. A., Gakuya, D. W., Mbuthia, P. G., Mande, J. D., Afakye, K., & Maingi, N. (2016). Myiasis in dogs in the Greater Accra region of Ghana. Vector-Borne and Zoonotic Diseases, 16, 54–57. https://doi.org/10.1089/vbz.2015.1811
- Madeira, N. G., Silveira, G. A. R., & Pavan, C. (1989). The occurrence of primary myiasis in cats caused by Phaenicia eximia (Diptera: Calliphoridae). Memórias do Instituto Oswaldo Cruz, 84, 341. https://doi.org/10.1590/S0074-02761989000800060
- McNae, J. C., & Lewis, S. J. (2004). Retrospective study of Old World screwworm fly (Chrysomya bezziana) myiasis in 59 dogs in Hong Kong over a one year period. Australian Veterinary Journal, 82, 211–214. https://doi.org/10.1111/j.1751-0813.2004.tb12677.x
- Mendes-de-Almeida, F., Labarthe, N., Guerrero, J., Landau-Remy, G., Rodrigues, D. P., Borja, G. E., & Pereira, M. J. (2007). Cochliomyia hominivorax myiasis in a colony of stray cats (Felis catus Linnaeus, 1758) in Rio de Janeiro, RJ. Veterinary Parasitology, 146, 376–378. https://doi.org/10.1016/j.vetpar.2007.02.021
- Morris, O. S., & Titchener, R. N. (1997). Blowfly species composition in sheep myiasis in Scotland. Medical and Veterinary Entomology, 11, 253–256. https://doi.org/10.1111/j.1365-2915.1997.tb00403.x
- Moshaverinia, A., & Kazemi Mehrjerdi, H. (2016). Canine myiasis and its causal agents in northeastern Iran. Iranian Journal of Parasitology, 11, 91–97.
- Muñoz-García, C. I., Lorenzo-Burgunder, D., Gumi-Castillo, G., Perelló-Undreiner, D. B., Zenteno-Nava, E., & Orozco-Gregorio, H. (2016). Canine myiasis by Lucilia eximia in North America. Tropical Biomedicine, 33, 494–499.
- Ogo, I. N., Mwansat, G. S., Jambalang, A., Ogo, M. F., Onovoh, E., Ogunsan, E. A., Dogo, G. I., Banyigyi, S., Odoya, E. M., Chukwu, O. O. C., Yako, A. B., & Inyama, P. U. (2005). Retrospective study on the prevalence of canine myiasis in Jos - South Local Government area of Plateau State, Nigeria. Journal of Pest Disease and Vector Management, 6, 385–390.
- Ogo, N. I., Onovoh, E., Ayodele, D. R., Ajayi, O. O., Chukwu, C. O., Sugun, M., & Okeke, I. O. (2009). Cutaneous canine myiasis in the Jos metropolis of Plateau State, Nigeria, associated with Cordylobia anthropophaga. Veterinarski Arhiv, 79, 293–299.
- Orfanou, D. C., Papadopoulos, E., Cripps, P. J., Athanasiou, L. V., & Fthenakis, G. C. (2011). Myiasis in a dog shelter in Greece: Epidemiological and clinical features and therapeutic considerations. Veterinary Parasitology, 181, 374–378. https://doi.org/10.1016/j.vetpar.2011.04.006
- Patton, W. S. (1920). Some notes on Indian Calliphorinae. part I Chrysomyia bezziana Villeneuve, the common Indian Calliphorinae whose larvae cause cutaneous myiasis in man and animals. Indian Journal of Medical Research, 8, 17–29.
- Pekmezci, D., Pekmezci, G. Z., Açici, M., Gökalp, G., & Tütüncü, M. (2014). A case of auricular, anal and umbilical myiasis caused by the larvae of Phormia regina (Meigen) (Diptera: Calliphoridae) in neonatal kittens. Türkiye Parazitoloji Dergisi, 38, 71–75. https://doi.org/10.5152/tpd..2014.3275
- Pezzi, M., Whitmore, D., Bonacci, T., Del Zingaro, C. N. F., Chicca, M., Lanfredi, M., & Leis, M. (2017). Facultative myiasis of domestic cats by Sarcophaga argyrostoma (Diptera: Sarcophagidae), Calliphora vicina and Lucilia sericata (Diptera: Calliphoridae) in northern Italy. Parasitology Research, 116, 2869–2872. https://doi.org/10.1007/s00436-017-5582-z
- Pezzi, M., Whitmore, D., Chicca, M., Lanfredi, M., & Leis, M. (2015). Traumatic myiasis caused by an association of Sarcophaga tibialis (Diptera: Sarcophagidae) and Lucilia sericata (Diptera: Calliphoridae) in a domestic cat in Italy. Korean Journal of Parasitology, 53, 471–475. https://doi.org/10.3347/kjp.2015.53.4.471
- Principato, M., & Cioffi, A. (1996). Notes on the incidence of the Lucilia genus (Diptera: Calliphoridae) in Umbria, Central Italy. A case of myiasis by Lucilia ampullacea (Villen 1922) in Testudo graeca. Proceedings of the 20th International Congress of Entomology. August 25 to 31, Florence, Italy. p. 769.
- Principato, M., Pepe, M., Arcelli, R., & Polidori, G. A. (1994). Myiasis in a dog in Umbria by Sarcophaga haemorrhoidalis (Fallen) (Diptera: Sarcophagidae): A fly infecting also man. Parassitologia, 36(Suppl. 1), 117.
- Rauchbach, K., & Hadani, A. (1972). Hauntmyiasis bei Gans und Hund durch die Goldfliegenart Lucilia sericata (Meigen 1826). Deutsche Tierärztliche Wochenschrift, 79, 365–366.
- Rawlins, S. C. (1985). Current trends in screwworm myiasis in the Caribbean region. Veterinary Parasitology, 18, 241–250. https://doi.org/10.1016/0304-4017(85)90050-0
- Rawlins, S. C., Alexander, F. C., Moe, V., Caesar, E., Moll, K., & Applewhaite, L. (1983). Screwworm (Diptera: Calliphoridae) myiasis in the southern Caribbean, and proposals for its management. Journal of Economic Entomology, 76, 1106–1111. https://doi.org/10.1093/jee/76.5.1106
- Ribbeck, R., Schroder, E., & Schumann, H. (1979). Lucilia-sericata-Larven als Erreger von Wundmyiasis bei Hund und Katze. Monatshefte Für Veterinärmedizin, 34, 383–384.
- Robbins, K., & Khachemoune, A. (2010). Cutaneous myiasis: A review of the common types of myiasis. International Journal of Dermatology, 49, 1092–1098. https://doi.org/10.1111/j.1365-4632.2010.04577.x
- Rodríguez, J. M., & Pérez, M. (1996). Cutaneous myiasis in three obese cats. Veterinary Quarterly, 18, 102–103. https://doi.org/10.1080/01652176.1996.9694627
- Rutland, B. E., Byl, K. M., Hydeskov, H. B., Miniter, B., & Johnson, C. A. (2017). Systemic manifestations of Cuterebra infection in dogs and cats: 42 cases (2000–2014). Journal of the American Veterinary Medical Association, 12, 1432–1438. https://doi.org/10.2460/javma.251.12.1432
10.2460/javma.251.12.1432 Google Scholar
- Schnur, H. J., Zivotofsky, D., & Wilamowski, A. (2009). Myiasis in domestic animals in Israel. Veterinary Parasitology, 161, 352–355. https://doi.org/10.1016/j.vetpar.2009.01.026
- Scholl, P. J., Catts, E. P., & Mullen, G. R. (2009). Myiasis (Muscoidea, Oestroidea). In G. Mullen, & L. Durden (Eds.), Medical and veterinary entomology, 2nd ed. (pp. 309–338). Academic Press, Elsevier.
- Sevgili, M., Altaş, M. G., & Gökçen, A. (2009). Bir köpekte oral myiasis olgusu. Türkiye Parazitoloji Dergisi, 33, 92–94.
- Singh, A., & Singh, Z. (2015). Incidence of myiasis among humans - a review. Parasitology Research, 114, 3183–3199. https://doi.org/10.1007/s00436-015-4620-y
- Singh, D., & Singh, A. (2007). A study on the incidence of myiasis among pet dogs in the state of Punjab. Journal of Punjab Academy of Sciences, 4, 99–102.
- Supperer, R., & Hinaidy, H. K. (1975). Myiasis bei Mensch und Tier in Österreich. Wiener Tierärztliche Monatsschrift, 62, 255–258.
- Szpila, K. (2012). Key for identification of European and Mediterranean blowflies (Diptera, Calliphoridae) of medical and veterinary importance - adult flies. In D. Gennard (Ed.), Forensic Entomology, an introduction, 2nd ed. (pp. 77–81). Wiley-Blackwell.
- Tannahill, F. H., Coppedge, J. R., & Snow, J. W. (1980). Screwworm (Diptera: Calliphoridae) myiasis on Curaçao: Reinvasion after 20 years. Journal of Medical Entomology, 17, 265–267. https://doi.org/10.1093/jmedent/17.3.265
- Verocai, G. G., Fernandes, J. I., Correia, T. R., de Souza, C. P., Melo, R. M. P. S., & Scott, F. B. (2010). Furuncular myiasis caused by the human bot-fly Dermatobia hominis in a domestic cat from Brazil. Journal of Feline Medicine and Surgery, 12, 491–493. https://doi.org/10.1016/j.jfms.2009.12.019
- Vignau, M. L., & Arias, D. O. (1997). Myiasis cutáneo-ulcerosas en pequeños animals. Parasitología Al Día, 21, 36–39.
- Wall, R., & Lovatt, F. (2015). Blowfly strike: Biology, epidemiology and control. In Practice, 37, 181–188. https://doi.org/10.1136/inp.h1434
- Wendell Snow, J., Coppedge, J. R., Baumhover, A. H., & Gorsira, R. (1978). The screwworm Cochliomyia hominivorax (Diptera: Calliphoridae) reinfests the island of Curaçao, Netherlands Antilles. Journal of Medical Entomology, 14, 592–593. https://doi.org/10.1093/jmedent/14.5.592
- Zumpt, F. (1965). Myiasis in man and animals in the world. Butterworth & Co.
Citing Literature
