Tropical Biomedicine 33(3): 494–499 (2016)

Canine myiasis by eximia in North America

Muñoz-García, C.I.1*, Lorenzo-Burgunder, D.2, Gumi-Castillo, G.2, Perelló-Undreiner, D.B.2, Zenteno-Nava, E.2 and Orozco-Gregorio, H.3,1 1Departamento de Producción Agrícola y . Universidad Autónoma Metropolitana-Unidad Xochimilco, Mexico. Calz. del Hueso 1100, Col Villa Quietud Del Coyoacán. CP 04960, Mexico City, México 2Licenciatura en Medicina Veterinaria y Zootecnia. Universidad del Valle de México, México. San Juan de Dios No. 6 Ex-Hacienda de San Juan, C.P. 14370, Tlalpan, Mexico City, Mexico 3Facultad de Agronomía y Veterinaria. Universidad Autónoma de San Luis Potosí, México. Carretera San Luis- Matehuala Km. 14.5, Soledad de Graciano Sánchez, C.P. 78321, San Luis Potosí, San Luis Potosí, Mexico *Corresponding author e-mail: [email protected] Received 4 December 2015; received in revised form 17 June 2016; accepted 10 July 2016

Abstract. Myiasis is the invasion of Diptera larvae in live vertebrates tissues. It has been registered in tropical areas, but not in urban of North America. Moreover, there is no information about lesions description, laboratory tests, and treatment applied to canines. We report a myiasis located in the dorsum of an overweight male canine. larvae were identified as Lucilia eximia, an opportunistic species that scarcely infest live vertebrates, and with no records in North America animals before. Abnormalities of complete blood count like leukocytosis by neutrophilia and serum biochemical changes like elevations in alanine aminotransferase, aspartate aminotransferase, creatine kinase, globulins and amylase were detected. Because Lucilia is characterized by lower host-specificity and infestation outbreaks occur worldwide, it is imperative to continue increasing the understanding of Lucilia myiasis, its clinical presentation, risk factors, therapy and correct entomological classification. Otherwise, more cases could occur in animals and humans.

INTRODUCTION Giangaspero et al., 2011), and risk factors for animals and humans include open wounds, Myiasis is the invasion of Diptera larvae in poor hygiene, advanced age, vascular live vertebrates tissues, causing traumatic occlusive disease, and the inability to injuries of cutaneous tissue, body cavities discourage from depositing eggs or and organs. Diptera associated with this larvae because of physical impairment pathology are blow flies (), (Sanford et al., 2014). However, no flesh flies (Sarcophagidae) and bot flies information exists about description of (Oestridae). Whereas Oestridae is composed lesions, laboratory tests and treatment in by obligated parasites, Calliphoridae and canines. Sarcophagidae are not (Zumpt, 1965). In pets, maggots affect dogs, rabbits and cats in a lesser extent (Anderson & Huitson, 2004). CASE HISTORY Myiasis is well registered in tropical areas, and not in urban companion animals from In September of 2013 an 8 year-old North American temperate zones. overweight male Pembroke Welsh Corgi Nevertheless, records of canine myiasis by (PWC) from Mexico City Metropolitan Area, Sarcophagidae flies exist in livestock areas was presented with pale gums and larval of Italy, Morocco and Hungary. Ears, legs and infestation located on the dorsum (Fig. 1a). genitals are the most frequently affected Dog owner referred a two-days history of anatomical regions (Farkas et al., 2009; inappetence, depression and fetid odor.

494 Maggots were unnoticed by owner because (122 U/L, reference range <70 U/L), aspartate the patient had dense coat, a Corgi variety aminotransferase (69 U/L, reference range commonly named “fluffy Corgi”. Under <55 U/L), triglycerides (1.28 mmol/L, general anesthesia with isoflurane dorsal reference range 0.57–1.14 mmol/L), creatine area was shaved, and then skin lesions were kinase (773 U/L, reference range <213 U/L), observed. Fig. 1b shows the extensive globulins (43.0 g/l, reference range 23.5– ulceration of the skin with purulent exudate 39.1 g/l) and amylase (6373 U/L, reference and necrotic tissue. range <1100 U/L) and decrease in albumin Larvae were manually removed, killed (25.0 g/L, reference range 29.1–39.7 g/L) and in hot water (>80ºC), fixed in 70% alcohol, albumin/globulin ratio (0.6, reference range and further microscopically identified as 0.78–1.46). The patient was hospitalized Lucilia eximia (Wiedemann, 1830) based on for 3 days. Wounds were cleaned daily morphological characters described by with povidone-iodine and chlorhexidine, Florez and Wolff (2009), i.e. shape and size and the pharmacological treatment was of posterior spine bands, spiracles and metronidazole (Otrozol 500; Pisa cephalopharyngeal skeleton (Fig. 2). Laboratories®; 60 mg/kg BW, q24h) and Maggots were at the same developmental ivermectin (Iverfull; Aranda Laboratories®; stage (L3), indicating no successive 200 µg/kg BW, one dosage). At the fourth infestation. Biochemical profile and day the dog followed antibiotic treatment complete blood count were performed. with enrofloxacin (Enroxil; Senosiain Findings on complete blood count included Laboratories®; 10 mg/kg PO, q24h) for 10 days leukocytosis (25.7 x 109/L, reference range at home. After one month, wounds were 6.0–17.0 x 109/L) by neutrophilia (21.8 x completely healed and repeated blood tests 109/L, reference range 3.0–11.5 x 109/L). indicated no alterations in the biochemical Serum biochemical abnormalities were profile and blood count. elevation in alanine aminotransferase

Figure 1. Dorsal cutaneous myiasis by Lucilia eximia in a Pembroke Welsh Corgi. (1a) Dorsal view with larva infestation, the arrows shows alive maggots. (1b) Skin lesions viewed after shaving. (1c and 1d) Healed wound.

495 Figure 2. Lucilia eximia larvae. (2a) Lucilia eximia third-stage larvae. (2b) Caudal view of the larvae with posterior spiracles located centrally. (2c) Posterior spiracle. (2d) Cephalopharyngeal skeleton (magnification, x4).

DISCUSSION attracted by wounds of sick, injured or moribund animals; however, records of Herein, we report the first case of primary attack on healthy animals exist in South myiasis of L. eximia in the dorsal area of an America during hot months (Azeredo-Espin adult dog from a temperate city of North & Madeira, 1996). The infestation in the America. L. eximia is a necrophagous blow PWC occurred in late summer, which is , distributed in rural, urban, and forest congruent with the season when several habitats from United States to Argentina; the species of maggots attack humans and farm oviposition temperature in L. eximia ranges and companion animals in United States, Italy from 26 to 28.8ºC, and the adult fly is primary and Israel (Giangaspero et al., 2011; Schnur attracted to a wide variety of substrates such et al., 2009; Sherman, 2000). Myiasis caused as garbage, carcasses, and scats for food by L. eximia has been reported in tropical and oviposition (Kirkpatrick & Olson, 2007). zones of Brazil, in urogenital region and It also acts as facultative ectoparasite abdomen of young animals, a puppy and a

496 kitten of 10 and 15 days old respectively parasite, and host and environmental (Azeredo-Espin, 1996). According to characteristics that favour its occurrence. Anderson and Huitson (2004), presence of Information on the genus refers primarily traumatic cutaneous myiasis is associated to L. sericata and L. cuprina. Larvae of with neglected dogs with insufficient daily L. cuprina can excrete ammonium that care. Therefore, L. eximia colonization becomes toxic nonionized ammonia at the success in PWC could be attributed to a wound site and in the blood. High blood suitable environment generated by dense concentration of nonionized ammonia and bad groomed coat, backyard life, rainy causes reduction of mature neutrophils, season and obesity. Fatness is a predisposing lymphocytes, eosinophils and serum globulin factor of being parasitized by larval flies (Otranto, 2001). Changes in circulating previously reported in cats (Rodríguez & neutrophils, lymphocytes, eosinophils and Pérez, 1996), but physiological factors behind serum globulin found in the present are not that association have not yet explained. in conformity with previously reported in Recently, a case of human infestation by L. L. cuprina, and this maybe was related eximia was first reported in a presumably to concomitant antigen response. The necrotic leg of an elderly homeless from hematological results show leukocytosis with United States and the probable cause of neutrophilia induced by inflammatory infestation was that his extremity was cooler response, possibly caused by associated than the rest of the body, favoring colonization pyogenic bacteria. This finding has been and larval development (Sanford et al., 2014). previously reported in severe cases of human Here, we hypothesize that a lower trunk wound myiasis accompanied by secondary temperature, caused by obesity and a wet and infection (Kaczmarczyk et al., 2014), and in dense fur, was the primary predisposing twenty-two canine patients with dorsal factor; because in the case of necrophagous furunculosis, including 3 PWC, many of them parasites, previous studies demonstrated that associated with Pseudomonas aeruginosa low host temperature improve the parasite (Cain & Mauldin, 2015). Cutaneous myiasis chances of locating a host (Wharton, 1999). is frequently complicated by concurrent Savastano et al. (2009) confirm that obese bacterial infection and the most common humans show lower skin temperatures in isolated are Pseudomonas spp. and trunk than in peripheral regions. The effect Staphylococcus intermedius in sheep and was attributed to the insulating layer of cats, respectively (Otranto, 2001; Rodríguez subcutaneous adipose tissue that impedes & Pérez, 1996). PWC successful treatment heat loss across skin. This effect is higher response was attributed to the use of broad- in body areas of increased fat, like dorsum; spectrum antimicrobials and antiparasitic and enhanced temperature reduction could drugs. Enrofloxacine is a systemic anti- occur on dorsal region for the influence of microbial drug commonly used in treatment excessive humidity on the dense and bad- of bacterial skin infections (Beco et al., 2013), groomed coat. Wet fur is a poor insulator and Ivermectin has been used successfully because water increases conductivity eliminating blow flies in domestic cats causing to lose heat faster than dry fur (Rodríguez & Pérez, 1996). Presence of serum (Dickerson et al., 2012). chemistry abnormalities like increased There are few data available concerning levels of aspartate aminotransferase, alanine the systemic and immune response to aminotransferase and creatine kinase cutaneous myiasis compared with the typically indicate major muscle damage, response to other ectoparasites (e.g. fleas and when liver pathology is excluded (Valentine ticks), then some complete blood count and et al., 1990). Skin pathologies caused by serum biochemical abnormalities found in L. eximia in PWC correspond to those PWC cannot be easily explained. Limited described in sheep affected by L. cuprina information exists about development of (Otranto, 2001). Studies in L. cuprina disease, biology of L. eximia acting as demonstrate that feeding maggots will

497 aggressively invade tissue through the skin REFERENCES dermis and deeper layers, like muscle, with the help of proteolytic enzymes discharged Anderson, G.S. & Huitson, N.R. (2004). in larval excretory-secretory products (one Myiasis in pet animals in British chymotryptic and two tryptic). The activity Columbia: The potential of foresic of these enzymes with elastase and plasmin entomology for determining duration of substrates suggested their involvement in possible neglected. Canadian Veterinary the immunopathogenesis of cutaneous Journal 45: 993-998. lesions (Otranto, 2001), and concomitant Azeredo-Espin, A.M.L. & Madeira, N.G. systemic response, like increase of liver (1996). Primary myiasis in dog caused transaminases and creatine kinase. Other by Phaenicia eximia (Diptera: abnormalities as increased plasma Calliphoridae) and preliminary mito- triglycerides and amylase could be chondrial DNA analysis of the species in associated with obesity. Brazil. Journal of Medical Entomology Attention should be paid to new cases 33: 839-843. of L. eximia myiasis in domestic animals; Beco, L., Guaguère, E., Méndez, C.L., Noli, C., especially those living in close proximity to Nuttall, T. & Vroom, M. (2013). Suggested persons, because it could represent a guidelines for using systemic anti- potential source for human infestation; microbials in bacterial skin infections: especially in high-risk groups such as part 2 – antimicrobial choice, treatment homeless people and patients at risk of regimens and compliance. Veterinary diabetic foot. The first case of L. eximia Record 172: 156-160. myiasis in human occurred in a homeless Cain, C.L. & Mauldin, E.A. (2015). Clinical from United States (Sanford et al., 2014), and and histopathologic features of dorsally more cases could occur because Lucilia located furunculosis in dogs following shows low host-specificity. Other Lucilia water immersion or exposure to species infest humans and outbreaks occur grooming products: 22 cases (2005– worldwide. For example, 35 cases of L. 2013). Journal of the American sericata wound myiasis have been reported Veterinary Medical Association 246: 522- in US until 2000 (Sherman, 2000). Sanity 529. experts and vets are inexperienced with Dickerson, A.K., Mills, Z.G. & Hu, D.L. maggots, and there is lack of knowledge (2012). Wet mammals shake at tuned about managing or preventing the disease frequencies to dry. Journal of the Royal in pets and humans. Then, is imperative to Society Interface 9: 3208-3218. continue increasing the understanding of Farkas, R., Hall, M.J.R., Bouzagou, K., myiasis, its clinical presentation, risk Lhor, A.K. & Khallaayoune, K. (2009). factors, therapy and correct entomological Traumatic myiasis in dogs caused classification. by Wohlfahrtia magnifica and its importance in the epidemiology of Acknowledgments. The authors would like wohlfahrtiosis of livestock. Medical and to thank Francisco Lorenzo-Geadah for their Veterinary Entomology 23: 80-85. valuable help with the clinical case and Florez, E. & Wolff, M. (2009). Descripción y Emilio Rendón-Franco for his critical review. clave de los estadios inmaduros de las We also appreciate Histopathology lab of principales especies de Calliphoridae UAM-Xochimilco for providing facilities for (Diptera) de importancia forense en entomological work. Colombia. Neotropical Entomology 38: 418-429.

498 Giangaspero, A., Traversa, D., Trentini, R., Savastano, D.M., Gorbach, A.M., Eden, H.S., Scala, A. & Otranto, D. (2011). Traumatic Brady, S.M., Reynolds, J.C. & Yanovski, myiasis by Wohlfahrtia magnifica in Italy. J.A. (2009). Adiposity and human regional Veterinary Parasitology 175: 109-112. body temperature. American Journal of Kaczmarczyk, D., Kopczyñski, J., Kwiecieñ, Clinical Nutrition 90: 1124-1131. J., Michalski, M. & Kurnatowski, P. Schnur, H.J., Zivotofsky, D. & Wilamowski, A. (2011). The human aural myiasis caused (2009). Myiasis in domestic animals in by Lucilia sericata. Wiadomosci Israel. Veterinary Parasitology 161: 352- parazytologiczne 57: 27-30. 355. Kirkpatrick, R.S. & Olson, J.K. (2007). Sherman, R.A. (2000). Wound myiasis in Nocturnal light and temperature urban and suburban United States. influences on necrophagous, carrion- Archives of Internal Medicine 160: 2004- associating blow fly species (Diptera: 2014. Calliphoridae) of forensic importance Rodríguez, J.M. & Pérez, M. (1996). Cutaneous in Central Texas. Southwestern myiasis in three obese cats. Veterinary Entomologist 32: 31-36. Quarterly 18: 102-103. Otranto, D. (2001). The immunology of Valentine, B.A., Blue, J.T., Shelley, S.M. & myiasis: parasite survival and host Cooper, B. (1990). Increased serum defense strategies. Trends in Para- alanine aminotransferase activity sitology 17: 176-182. associated with muscle necrosis in the Sanford, M.R., Whitworth, T.L. & Phatak, D.R. dog. Journal of Veterinary Internal (2014). Human wound colonization by Medicine 4: 140-143. Lucilia eximia and Chrysomya Wharton, D.A. (1999). Parasites and low rufifacies (Diptera: Calliphoridae): temperatures. Parasitology 119: S7-S17. myiasis, perimortem, or postmortem Zumpt, F. (1965). Myiasis in Man and colonization? Journal of Medical Animals in the Old World. A Textbook Entomology 51: 716-719. for Physicians, Veterinarians and Zoo- logists.

499