Obligatory Myiasis-producing Flies
Many dipteran flies produce larvae that must lead a parasitic existence and result in obligatory myiasis. Only one fly in North America, Cochliomyia hominivorax, is a primary invader of fresh, uncontaminated skin wounds of domestic animals. Another species of screwworm, Chrysomya bezziana, is found in Africa and southern Asia, including Papua New Guinea.
(Primary screwworm, New World screwworm)
Cochliomyia hominivorax is distributed throughout the neoarctic and neotropical regions of the western hemisphere. As a result of massive state, federal, and international eradication programs, extant populations of C hominivorax are no longer found in the USA or Mexico; isolated reports are often traced to importation of infested animals from locations where the screwworm is still prevalent. Extant populations are found in Central and South America and in certain Caribbean Islands.
Adult female flies lay batches of 200–400 eggs in rows that overlap like shingles in a mass on the edge of a fresh wound. After 12–21 hr, larvae hatch, crawl into the wound, and burrow into the flesh. The larvae feed on wound fluids and live tissue. After 5–7 days, grown larvae exit from the wound, fall to the ground, and burrow in the soil to pupate. The pupal period varies from 7 days to 2 mo, depending on the temperature. Freezing or sustained soil temperatures <46°F (8°C) kill the pupae. Adults breed only once during their lifetime, a fact that can be used as an advantage in biologic control. Adult flies usually mate when 3–4 days old, and gravid females are ready to oviposit when ~6 days old. In warm weather, the life cycle may be completed in 21 days. Only female flies feed and oviposit on wounds; males and younger, virgin females gather to mate in vegetation, especially flowering vegetation.
Newly infested wounds contain screwworm larvae of a single age; older, larger wounds may contain larvae of various ages and of different species of flies. The malodorous, reddish brown fluid produced in the wound usually drains and may stain the hair or wool around or below the wound. As annoyance increases, the infested animal seeks protection by retreating to the densest available shade. Even a small and relatively inconspicuous wound infested with screwworm larvae attracts not only more screwworm flies but also facultative myiasis-producing flies. Necrotic tissues attract even more flies. The wound can become greatly enlarged due to multiple infestation and, unless treated, usually results in death of the animal.
The parasitic larvae are tapered and have mouth hooks at the narrow end and breathing spiracles at the wide end. Body segments are ringed with spines. Fully grown larvae can be as long as 1.5 cm. Larvae are often identified by their “wood screw” shape and appearance and can be distinguished from the larvae of the facultative myiasis-producing flies by the darkly pigmented tracheal tubes on the dorsal aspect of the posterior end of third-stage larvae. These tubes can be easily visualized through the larval cuticle.
Adult screwworm flies are similar in appearance to other blow flies. The adult stage is never recovered in a veterinary case scenario. They are bluish to bluish green, have a reddish orange head and eyes, and are slightly larger than a house fly. If collected, they are difficult to distinguish from other blow flies or bottle flies. Identification of adult screwworms is probably best left to an entomologist.
Screwworm infestation must be reported to both state and federal authorities. C hominivorax has been eradicated from the USA but occasionally enters the country surreptitiously on imported animals. In the USA, if a wound is thought to be infested with screwworm larvae, the USDA can be contacted at http://www.aphis.usda.gov/index.shtml.
Screwworms in wounds can be killed by direct application of a wound dressing, called a smear. Such smears, which contain lindane or ronnel, may be difficult to find in the USA because of the eradication program. Smears are best applied with a 1-in. (2.5-cm) paint brush and should reach all of the many pockets formed by the burrowing larvae in deep wounds. A thin layer should also be applied to the skin surrounding the wound to protect it from reinfestation. Wounds may also be treated with aerosol, dust, or foam formulations of coumaphos, lindane, or ronnel. To protect animals from infestation and also to kill larvae in small wounds that are difficult to detect, animals can be sprayed thoroughly with ronnel or sprayed with or dipped in coumaphos.
In 1958, the USDA initiated a program in the southeastern states to eliminate screwworms by the sterile male release technique. When reared artificially and exposed to irradiation shortly before they emerge from the pupae, male flies are able to mate but sterile. The female mates only once and, when mated with a sterile male, lays eggs that do not hatch. Therefore, release of sufficient numbers of sterile males in an area throughout a period of time leads to eradication. By 1959, screwworms had been eliminated from Florida.
This program was expanded to cover the rest of the area involved in the USA and then, via a joint Mexico-–USA agreement, to include most of Mexico. This, along with the use of screwworm attractant and an insecticide system that attracted and killed adults, led to eradication of screwworms from Mexico. There is interest in expanding this area throughout Central America and the Caribbean. However, until this has been achieved, constant vigilance by all who deal with animals in the southern USA and Mexico is necessary to detect an infestation quickly and to eradicate it before the flies reproduce and spread.
(Old World screwworm, Oriental fly, Bezzi’s blow fly)
Chrysomya bezziana is found in Africa, the Indian subcontinent, and southeast Asia from Taiwan in the north to Papua New Guinea in the south. This fly is not indigenous to Australia. Owing to its geography, the most likely potential port of entry for C bezziana to the USA is Hawaii.
Adult screwworms are usually not seen in the field. The adult fly has a dark metallic green body with abdominal segments with narrow bands along the posterior margins. The legs are black or partially brown. The face is orange/yellow. The first larval stage probably goes unnoticed because of its small size, as long as 3 mm at the time of its molt to the second stage. The second stage is quite similar to the third but is 4–9 mm long. The third-stage larvae are large, as long as 18 mm. The body is composed of 12 segments that have broad encircling bands of spinules. All three stages are maggot-like in their appearance and have posterior spiracles that are unique to the species. The posterior end of the larva has its spiracular plate located in a deep cleft at the end of the eighth abdominal segment. The spiracular plates are large and well separated. The peritreme and the three breathing slits are wide.
C bezziana produce a particularly vile myiasis. Female flies are attracted to open wounds of people and domestic and wild animals, laying their eggs in masses of 150–500 at the edge of wounds or near body orifices. Larvae develop to the third stage ~2 days after hatching. They burrow deep into the wound such that only their posterior ends are visible. The entire larval stage lasts 5–6 days. The pupal stage lasts 7–9 days in tropical conditions and longer in cooler environments. The adult flies emerge later to mate, locate a new host, and continue the cycle. Female flies mate only once during their lifetime—a fact paramount in prevention and control. Under favorable conditions, there may be ≥8 generations per year.
The larvae of C bezziana are obligatory wound parasites, never developing in carcasses or decomposing organic material. Although female flies are attracted to open wounds, occasionally eggs are deposited on the unbroken, soft skin of various parts of the body, especially if contaminated by blood or mucous discharge. When the larvae hatch, they burrow into the flesh of the host, using their hooked mouthparts to scrape away at the tissues and lacerate the fine blood vessels. Larvae are voracious blood feeders. During the bloodsucking phase, only the caudal ends of the maggots with their blackish peritremes remain visible at the surface of the lesion, enabling the larvae to breathe. As many as 300 maggots have been seen in some wounds. In untreated wounds, the destructive activity of the larvae may lead to the death of the animal within a very short time. Secondary infestation with the facultative myiasis-producing flies (see Facultative Myiasis-producing Flies) may complicate treatment and control.
The identification of the rarely observed adult flies and their associated larval stages is best left to an entomologist. A definitive diagnosis can be made only after observation, extraction, and identification of typical larvae. Diagnosis may often be made by residence in or history of travel to an area endemic for C bezziana. If a wound is thought to be infested with larvae of C bezziana, samples should be collected and sent to appropriate eradication officials.
Treatment of screwworm infestation involves killing the larvae in the lesions, promoting healing, and preventing secondary reinfestation with larvae of the facultative myiasis-producing flies. The extent of the lesions is determined by clipping the hair coat and removing as many larvae as possible. The larvae that are removed should be killed to prevent them from pupating and developing into adults. Larvae located deep within tissues must be extracted.
Ivermectin at dosages of 50, 100, and 300 mcg/kg administered to infested cattle resulted in 100% larval mortality for at least 6, 12, and 14 days, respectively. Depending on their age, larvae survived in established strikes after treatment at 200 mcg/kg. Mortality was 100% in larvae up to 2 days old but less in older larvae. However, many of the larvae that survived ivermectin therapy failed to develop to the adult stage. After treatment with 200 mcg/kg, residual protection lasted 16–20 days, 2–3 times that of most insecticide smears.
All wounds on domestic animals should be properly dressed, and all elective surgical procedures avoided during the fly season.
The fact that the female flies mate only once during their lifetime is an important fact to consider in the control of C bezziana. Pupal flies exposed to irradiation lead to sterile adults that can be released to mate with wild male and female flies. As a result, no viable offspring are produced in the wild.
Larvae of the genus Cuterebra are often referred to as wolves, warbles, rabbit bots, or rodent bots. These fly larvae infest the skin of rabbits, squirrels, mice, rats, chipmunks, and occasionally dogs and cats. (For clinical findings, diagnosis, and treatment, see Cuterebra Infestation in Dogs and Cats.)
The gray flesh fly, Wohlfahrtia vigil, is responsible for cutaneous myiasis in North America, particularly in southern Canada and the northern part of the USA. The adult flies have been recorded from the New England states to Alaska, but most reports are from eastern sections of Canada and the neighboring northeastern parts of the USA. All reports of infestation are in the skin of healthy animals, particularly the unbroken skin of the young.
All three larval stages are maggot-like in their appearance and have posterior spiracles unique to the species. The first larval stage is 1.5 mm at hatching and grows to 3.5 mm at the time of its molt to the second stage. The third stage is 7–18.5 mm long. Its posterior end is narrow, and it is covered with many irregular rows of small spines that have dark points and are directed posteriorly. This larva is better adapted to maintain an attachment to living tissues. The oral hooks are strongly developed. The posterior end of the larva has its spiracular plate located in a deep pit formed by the margins of the segment. The posterior spiracles have wide slits and a strong peritreme.
The gray flesh fly is larviparous—it deposits larvae instead of eggs on healthy, uninjured skin of suitable hosts, particularly young animals. Larvae penetrate the unbroken skin and form a boil-like (furuncular) swelling. Development to the infective third-larval stage is usually completed in 9–14 days. The parasites then drop to the ground and pupate for ~11–18 days, varying with the season of the year and the temperature. When cold weather approaches, the pupation period is greatly prolonged. Under laboratory conditions, it has been observed to last 7 mo. Parasites survive the winter in pupal form. Adults emerge and mate after ~3–4 days. Female flies begin larviposition ~1 wk later, depositing 6–16 larvae at a time. Female flies live for 35–40 days; males seldom survive >3 wk.
Female W vigil deposit active larvae near or directly on the host. Although larvae usually penetrate unbroken skin, in small animals, penetration may go deeper than the dermal tissue, even into the coelomic cavity.
The first indication that an animal is infected is exudation of serum and matting of the hair coat over the site of penetration. In light-skinned animals, a small inflammatory area, with a tiny hole visible in the center or to one side, is noticeable. These lesions may be palpated as they develop. On the third or fourth day, the larvae are 1.5–2 cm long and produce abscess-like lesions resembling those of Hypoderma spp in cattle. These lesions vary in size, shape, position, and the number of larvae they contain. The hair coat often becomes parted over the summit of the lesions and reveals an opening 2–3 mm in diameter. The posterior aspect of the larva is visible in these openings, through which it breathes. Openings are generally circular and well-defined; however, if several larvae are present in a single lesion, the shape of the opening is quite variable. Small animals infected with ≥5 larvae for several days become emaciated, and the skin becomes dry and loses its luster.
The penetration of the skin by the larvae, their development in the subcutaneous tissues, and secondary bacterial infection produce intense irritation and inflammation. Attempts by the animal to remove the larvae or relieve the irritation tend to aggravate the condition. Young animals may die from exhaustion. It has also been suggested that the larvae may produce toxic secretions. W vigil has been isolated from the skin of young children, particularly infants.
Adult gray flesh flies are nonparasitic and as a result will probably not be seen by owners or veterinarians. They are large grayish flies (~13 mm long), about twice the size of a house fly. The dorsal surface of the thorax is marked with three longitudinal bands, and the dorsal surface of the abdomen has three well-defined rows of oval black spots that are confluent with one another.
The identification of adult flies and their associated larval stages should be left to an entomologist. The presence of a dermal swelling with a central opening may lead to a tentative diagnosis of myiasis due to W vigil. A definitive diagnosis can be made only after extraction and identification of a typical larva. Extensive descriptions and dichotomous keys for the three larval stages are available. A tentative diagnosis may often be made by a history of either residence in or travel to a geographic area endemic for W vigil.
Larvae must be extracted from the skin. Applying heavy oil, liquid paraffin, or petrolatum jelly to the opening of the lesions will occlude the airway of the larvae. Applying a small amount of chloroform or ether to the opening may be helpful before removing larvae with forceps. Lidocaine hydrochloride can also be injected into the furuncular lesion to facilitate extraction. Great care should be taken during the extraction process to avoid rupturing larvae in situ, although anaphylaxis has not been reported. Antibiotics should be prescribed.
W vigil often infects young mink. A teaspoon of ronnel can be placed in the bedding of mink nest boxes as a control measure; however, ronnel should not be used in the bedding of kits <3 days old. Protection can be provided by using wire gauze to keep flies out of cages.
(Mango fly, Skin maggot fly, Ver du Cayor, Worms of Cayor)
The African tumbu fly, Cordylobia anthropophaga, is responsible for another boil-like (furuncular) myiasis in both people and animals in Africa, particularly in the sub-Saharan regions.
The adult flies are nonparasitic and as a result are not seen by owners or veterinarians. They are stout, compact flies, 6–12 mm long. They are light brown, with diffuse blue-gray patches on the thorax and dark gray on the posterior part of the abdomen. The face and legs are yellow. The second- and third-stage larvae are the stages usually seen in the animal’s skin.
Second-stage larvae are slightly club-shaped and exhibit large, black cuticular spines directed posteriorly and distributed irregularly over segments 3–8. Segments 9–11 are almost bare when compared with the preceding segments. The segments have a few rows of small, pale spines posteriorly. Segment 12 is densely covered with these spines. Segment 13 is indistinctly demarcated, lacking spines but possessing two pair of short processes. Each tracheal tube opens through two slightly bent slits. The second-stage larvae are 2.5–4 mm long. The size of advanced second-stage larvae varies greatly, as does the size of third-stage larvae. Fully mature larvae are 1.3–1.5 cm long. The body is cylindrical with 12 identifiable segments. Curved spines that are directed posteriorly are densely arranged at least up to segment 7; the last 5 segments may be either partially or densely covered with spines.
After fertilization, female flies produce 100–500 banana-shaped eggs, usually depositing them in dry, shady, sandy soil that has often been contaminated by urine or feces. Eggs are never deposited on the skin of the host. Eggs hatch after 1–3 days, and the larvae are initially 0.5–1 mm long. Larvae can survive as long as 15 days while waiting for a host and can penetrate the host in as little as 25 sec. After penetration, larvae reside in a cavity in the dermis and hypodermis. This cavity communicates to the external environment by means of a central breathing pore, which corresponds to the caudal end of the larva with its spiracles. A single larva is found in each cavity, within which the larva develops to the second and third stages. Larvae require 7–15 days to mature and then emerge through the breathing pore and drop to the ground, where they pupate. Adult flies emerge 10–20 days later, and the cycle begins again.
Rats and dogs are the usual definitive host; however, people, mice, monkeys, mongooses, squirrels, leopards, boars, antelopes, cats, goats, pigs, rabbits, guinea pigs, and chickens can be infested.
Clinically, the infestation is characterized by a small erythematous papule that appears 2–3 days after larval penetration. Within days, the papule enlarges until it becomes a nodule that resembles a boil (furuncle); hence, the description furunculoid myiasis. At the center of the nodule is a pore through which serous fluid oozes. This fluid can be hemorrhagic or purulent and contains larval feces.
Dogs with thin, soft skin seem to be more suitable hosts for larval development than dogs with thick skin. Preferential sites of infestation are the feet, genitals, tail, and axillae. In endemic areas, mild infestations in dogs do not produce clinical distress. Massive infestation may induce marked swelling and edema, especially if larvae are in close proximity to each other. Larvae can penetrate deep into tissues and cause considerable damage and even death.
The presence of a dermal swelling with a central opening may lead to a tentative diagnosis of myiasis due to C anthropophaga. A definitive diagnosis can be made only after extraction and identification of typical larvae. The identification of adult flies and their associated larval stages should be left to an entomologist.
A tentative diagnosis may often be made by a history of either residence in or travel to a geographic area endemic for C anthropophaga. However, the parasite has also been diagnosed in travelers and their accompanying pets from geographic areas where the parasite is not found.
Larvae can be removed by coating the breathing pore with a thick, viscous compound, such as heavy oil, liquid paraffin, sticking plaster, or petrolatum jelly. Clogging the pore causes the larva to become hypoxic and leave the cavity in search of oxygen. Light pressure at the edge of the lesion also aids in larval removal.
Lidocaine hydrochloride can be injected into the furuncular lesion to facilitate larval extraction with thumb forceps. Surgical excision is usually unnecessary and unwarranted while the larvae are alive but is used to remove dead or decaying larvae. Great care should be taken during the extraction process to avoid rupturing larvae in situ, although anaphylaxis has not been reported. Antibiotics should be prescribed.
Adult flies should be killed if seen indoors. Larvae should be removed from animals entering the house and destroyed. All rats should be killed and burned. Prevention of an infestation depends on cleanliness and regular disinfection of the animal’s sleeping quarters. In the case of valuable animals (eg, Angora rabbits), flies may be kept out of rabbit pens using wire gauze.
Because the adult female flies lay eggs in sandy soil contaminated by feces or urine, the parasite can be controlled in the pet’s environment by prompt removal of the pet’s feces and by covering urination sites on the premises with a layer of dirt.