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Cuterebra species

(Figures 4-57 through 4-)

ETYMOLOGY:Cutis = skin and terebro = to bore.

HISTORY: The genus Cuterebra was first described by Bracy Clark in 1815; however, the first published record is that of John Lawson (1709) in his book "A New Voyage to Carolina" (both cited in Sabrosky, 1986). The North American species of Cuterebra were described in detail by Sabrosky (1986) who provides an in-depth taxonomic description of each species that he considered valid. In this work, Sabrosky divided the genus Cuterebra into two subgenera: Cuterebra and Trypoderma. Cuterebra Cuterebra spp. are parasites of lagomorphs while Cuterebra Trypoderma spp. are parasites of rodents.

GEOGRAPHIC DISTRIBUTION: Western hemisphere, throughout the Americas. Fossils of Cuterebra that have been dated to be from 60 million years before the present have been recovered in North America (Townsend, 1942). There are maps showing collection sites of each North American species of Cuterebra in Sabrosky (1986).

According to Sabrosky (1986) there are 34 species of Cuterebra in North Ameria. There are 12 species in the subgenus Cuterebra and 22 species in the subgenus Trypoderma. Of the 12 members of the Cuterebra subgenus parasitic on rodents, three species, C. C. emasculator and C.C. fontinella, and C. C. americana, are found in the Eastern United States with the latter being more southern in distribution. Of the 22 species in the subgenus Trypoderma parasitic on lagomorphs, two species, C. T. abdominalis and C.T. buccata, are distributed throughout the eastern United States, one species, C. T. cuniculi, is restricted to the southeastern coastal areas, and one species, C. T. maculosa, is restricted to Panama and Guatamala. The remaining 27 species of Cuterebra are found in the western United States and in Mexico and Central America.

There are related genera, Metacuterebra, Pseudogametes, Rogenhofera and Andinocuterebra that parasitize rodents in South America. Also, the genus Alouttamyia is found in the necks of howler monkeys, Alouatta spp., and has been reported on several occasions from humans (Fraiha et al., 1984). None of these genera have been reported from cats.

LOCATION IN HOST: The larval stages of this parasite are commonly found in furuncular lesions in the skin of the rodent host. In the cat, these furuncular lesions may appear on the cheek, neck, top of the head, or on the thorax (Fischer, 1983). Larvae have also been reported from the nasal pharynx (Thirloway, 1982; Wolf, 1979), from the pharyngeal area (Kazacos et al., 1980), and from the orbit (Fischer, 1983) and anterior chamber of the eye (Johnson et al., 1988). Intracranial myiasis due to larval Cuterebra has been reported in cats on several occasions (Hendrix et al., 1989).

IDENTIFICATION: The adults are about the size and shape of bumble bees (Fig. 5-57). If one wants to identify the adult fly from a bot recovered from a warble, it will be necessary to allow the bot to pupate in some soil in a jar covered with a bit of screen or mesh; however, it has been found that bots from aberrant hosts often do not successfully pupate to the adult stage even under the best of conditions (Catts, 1982) The mature larva is characterized by its large size (about 3 cm) and the large spines on the segments (Fig. 5-59). These larvae also have spiracles that are distinctive of the genus with three serpentine openings forming what appears as three pie-shaped slices tracts within each spiraclular opening (Fig. 5-59) The spines on the anterior and posterior bands can be used to determine whether or not the larva is of the "rodent" or "lagomorph" subgenera (Sabrosky, 1986). The "rodent" bots have somewhat flattened, platelike spines, occasionally somewhat conical, usually bifid to many pointed in the anterior and posterior bands of spines on each segment. The mature larvae of the "rabbit" bots have conical, single-pointed spines, especially in the anterior and posterior bands on most segments (Fig. 5-60). The first and second instar larvae of the rodent and rabbit bots can be recognized by the large bands of dark spines that are present on the body segments (Fig. 5-61). These larvae have spiracles that are different from the mature third instar (Fig. 5-62).

In histological sections, the larvae of Cuterebra can be recognized by their large size and the spines on the surface of the body. Baird et al., 1989, describe the features that can be used to distinguish between the gnerea Cuterebra, Dermatobia, and Cordylobia in tissue sections.

LIFE CYCLE: Adult bot flies live only a few weeks, during which they mate and lay eggs (Figs. 5-63 & 5-64). Each day, male rodent botflies find and defend lek territories within botfly aggregation sites (Catts, 1994). When virgin females enter the area of congregation, they become conspicuous by making multiple flights over the summit. They are they chased by a male who will grab the female in midair with copulation being completed on land. Once the female has mated she then goes off to lay her eggs. The female bot fly lays her eggs in different locations depending on the species. The typical female will lay one to several thousand eggs, in groups of around 5-15 per site. Some species lay the eggs on grass stems, wood chips, and bark along narrow trails or rodent runs near the opening to the rodent burrow (similar methods are employed by the horse bots, Gasterophilus spp. when they attach eggs to the hairs of the face and legs of the horse), while other species actually enter the rodent burrow and lay their eggs within it.

Eggs of these bots hatch in response to sudden rises in temperature. The newly hatched larvae are moist and stick to the fur coats of passing rodents and lagomorphs. Hosts typically become infected by larvae entering some natural body opening (e.g., mouth, nose, eyes, or anus). It had been reported that larvae can enter through unbroken skin (Beamer and Penner, 1942; Penner, 1958), but this could not be repeated by other workers (Catts, 1982). Once within the rodent host, the larvae remain as first stages within the nasopharyngeal region for 6 to 8 days (Baird, 1975; Catts, 1967) where the small transparent larvae are found at the posterior end of the soft palate in the nasal passages of experimentally infected house mice and woodrats (Neotoma fuscipes). In these mice, the larvae remained quite small and transparent being only 2 to 3 times larger than the larvae that hatch from eggs. Work with other species of bots has shown that there may be a migration to the area of the trachea, migration through the tracheal wall into the thoracic cavity followed by migration through the diaphragm into the abdominal cavity prior to movement to their subcutaneous positions in the inguinal and thoracic areas (Gingrich, 1981). Once within the subcutaneous site, the larvae molt to the second instar and continue to grow within the developing warble. The molt to the third stage occurred around 17 to 19 days after infection in the case of C. latifrans (actually occurring about two days earlier in the house mouse). During the last 4 or 5 days of development, the larva enlarges the pore of the warble to make exit possible. It takes about 10 hours for the active larva to back out of the warble once the segments posterior to the spiracles are exposed. The time of larval maturation, from infection to when the larva leaves the warble, ranges from slightly less than 3 to over 8 weeks. The maturation time of the rodent bots seems to be on the average more rapid than that of the rabbit bots; the rodent bots tend to develop in three to four weeks while the rabbit bots tend to require 4 to 6 weeks.

Once the fully developed third-stage larva leaves the host, it burrows into the soil where pupation occurs. It may be anywhere from a month to several years before the adult fly emerges from the pupal case. Also, if larvae have developed in less than adequate hosts, there is a good chance that adult flies will not develop from the mature larvae, even after pupation (Catts, 1982).

The seasonality of infection is due to the timing of adult emergence in the late spring. Then, after 1 to 2 weeks for mating, the eggs are laid by the fertilized females. It then typically takes approximately 3 to 4 weeks for the warbles to become apparent. In the cooler climates, there is typically only one hatching of adults each year; however, in warmer climates, there is likely to be less ordered hatching of adult flies (Catts, 1982). There may be an occasional infection observed in winter in colder climates due most likely to eggs maintained within some protected location within the environment.

Cats probably become infected as they prowl in areas frequented by rodents and rabbits. It is possible for very young kittens to be infected with larvae crawling about on the queens fur. It is not known how the larvae enter the cat, but it would be assumed that they enter through the mouth, nose, or anus as they do in the rodent and lagomorph hosts.

CLINICAL PRESENTATION & PATHOGENESIS: Clinical signs depend largely on where the larvae have migrated. Cases tend to be more common during the mid-summer to fall months. The most common presentation is that of a subcutaneous warble (a 2 to 4 mm opening with well defined margins through the skin with a serosanguinous discharge). In these cases, the mature third-stage larva with its pair of large spiracles can be observed moving within the pore of the warble (Fig. 5-65). Most warbles occur around the face or neck; rarely, larvae may enter the globe of the eye causing chemosis, blepharospasm, serous occular discharge, and exudative uveitis with blindness. The larvae may be observed within the anterior chamber of the eye (Johnson et al, 1988; Fischer 1983). Some owners may observe the warble earlier in its development when the larva is smaller and often white to light cream colored. On these larvae, the dark body spines are clearly visible (Fig. 5-61). When extracted, the larva is found to be several centimeters long and often quite dark (Figs. 5-58 and 5-66). Typically, there are no signs of disease or distress in cats.

Those cats in which larvae migrate through the brain develop neurologic disease, the clinical signs of which depend on the migratory path of the larva. Clinical signs vary from acute onset of status epilepticus with no recovery, to multiple signs (head tilt, unilateral or bilateral central blindness, head pressing, dementia, continuous vocalization, abnormal placing reflexes, circling) designating multifocal CNS lessions, to only severe depressed mentation (Hendrix et al., 1989; McKenzie et al., 1978; Bennett et al., 1985; Cook et al., 1985). Many cats present in states of dementia, disorientation, and inappropriate responses to external stimuli Glass et al., 1998). After an acute onset, signs are usually rapidly progressive with a fatal outcome; more rarely, some cases may linger for weeks or months. Some cases bare a strinking similarity to the syndrome of feline ischemic encephalopathy (Cook et al., 1985; Summers et al., 1995). Although reported, it is uncommon for cats that develop neurologic disease to initially present with the cutaneous manifestations (warble) of infection (Hendrix et al, 1989). At necropsy, larvae may be observed intracranially (Fig. 5-67) or within the spinal cord (Figs. 5-68 and 5-69).

Some cats, after an acute onset of cerebral signs, recover and are left with residual signs of abnormal behavior, e.g., constant pacing or circling, abnormal mentation, or seizures. Occasionally spontaneous recovery appears to be complete.

Another typical presentation in cats can be signs of respiratory distress or upper respiratory disease. Some present with a history of sneezing and nasal discharge (sometimes for up to a weeks duration), unilateral facial swellings especially over the nose, extreme respiratory dyspnea sometimes with a bloody nasal discharge, and soft palate and pharyngeal swelling (Kazacos et al, 1980; Thirlaway, 1982; Wolf, 1979). Laryngeal edema resulting in laryngeal obstruction and respiratory arrest due to migration of a larvae in the cervical neck has been reported in a snow leopard (Ryan et al, 1990). Unlike cutaneous lesions, respiratory signs more often precede the development of neurologic signs (Cook et al., 1985; Personal Communication - SC Barr and A de Lahunta). Typically, if neurologic signs develop, they do so 1 to 2 weeks after respiratory signs, although respiratory signs may occur as long as 4 to 10 weeks before the onset of neurologic disease (Cook et al, 1985).

There seems to be a good indication that cerebrospinal cuterebriasis in cats is associated with or the cause of feline ischemic encephalopathy (Williams et al., 1998). This disease is not known to occur in areas where Cuterebra is not present, and it occurs most commonly at the same time of the year as cases of cuterebriasis. It is postulated that the vascular spasm associated with feline ischemic syndrome may be due to some toxin elaborated by the circulating fly larva.

DIAGNOSIS: Infections with Cuterebra in cats are typically observed in the late summer and early fall in those parts of North America that have cold enough winters to prevent year-round fly activity on a regular basis. A Cuterebra bot in a warble in the back of a cat is distinctive and diagnostic. Larvae migrating to cause neurologic or respiratory signs represent more of a challenge. The clinician should be suspicious of Cuterebra infection in cats developing severe upper respiratory disease (especially with unilateral signs of nasal discharge or nasal/facial swellings) during the late summer or fall months. Acute onset of neurologic disease sometimes preceded by a upper respiratory signs 1 to 2 weeks previously should provide strong suspicion of intracranial cuterebral myiasis. In some cats with upper respiratory signs, a leukocytosis with eosinophilia is pressent on peripheral hemograms. However, hemotology and serum biochemistry findings are usually nonspecific and but might help to rule out other diseases. If neurologic signs are present, cerebrospinal fluid analysis may show an elevation in protein, and pleocytosis with either neutrophils, mononuclear cells, or eosinophils. A CAT scan of an affected cat revealed a mottled appearance to the brain consistet with encephalitis, but no conclusive evidence of infection. Magnetic resonence immaging toreveal larvae or their migration tracks in the brain of affected animals appears to show promise, but as of yet images have not yet been published or the details of the observed lesions described (deLahunta, personal communication). In cases presenting with upper respiratory disease, examination of the pharynx, larynx, and nasal passages under general anesthesia may reveal a larvae.

TREATMENT: Treatment of cuterebriais currently requires the surgical extraction of the bot or bots. When mature bots are present within a warble, they are probably going to extract themselves very shortly, but they can be assisted in their leaving of the warble by the expansion of the pore and extraction with forceps, using care not to crush the bot. Squashing the larvae within the warble may result in a severe tissue reaction resulting from a Type I hypersensitivity-like reaction. Smaller and less developed larvae within the skin will require removal by careful dissection. Similarly, larvae within the soft tissues of the mouth, nasal sinus, larynx, or eye will require surgical extraction.

When larvae are present intracranially or within the spinal cord, the treatment of choice is likely to remain the extraction of the larva. As methods or radiographic imaging are improving, it may become possible to localize the developing larva and extract it. As of this time, however, no such success has been reported.

Ivermectin has been shown to be effective against Cuterebra species at 0.1 mg/kg, and is well tolerated when given at 0.3 mg/kg. Ivermectin (0.3 mg/kg subcutaneously on alternate days for 3 treatments) in association with corticosteroids has been reported in 2 cats with neurologic signs; in both cats the eventual outcome of the infection was not improved, although the larvae in 1 case at necropsy was decomposing (Hendrix et al., 1989).

At Cornell Veterinary College, a limited number of cats with the upper respiratory syndrome during late summer and fall have responded to the above regimen of ivermectin treatment (but given orally) combined with prednisone (1 mg/kg, PO, q 12 h for 3 weeks, then 1 mg/kg, PO, q 24 h for 3 weeks). Although the diagnosis has been presumptive, these cases improve and none to date have developed neurologic disease.

EPIZOOTIOLOGY: In the northern United States, most cases are observed in late summer and early fall; this is due to the univoltine life cycle of flies in these latitudes, i.e., flies only mate and lay eggs once a year. Thus, most rodents, rabbits, and cats are being infected at about the same time in the summer. Work at an aggregation site in Marin County, California, revealed that the most males of Cuterebra latifrons were present at the site around the end of August, although males were present from the beginning of June through the end of October (Catts, 1967). At an aggregation site in Pennsylvania, the most males of Cuterebra fontinella were present in the first haft of August, with males being present from mid to late June through the first half of september (Schiffer , 1983). The appearance of warbles in the late summer and early fall would coincide with the three to six weeks required for the larvae to reach the stage where they are ready to leave the host and pupate. In climates where the flies are multivoltine, there is the likely possibility that the seasonality of bot appearance would be less dramatic than in the cooler climes.

HAZARDS TO OTHER ANIMALS: The larva in the back of the cat is no hazard to either the handler or the other animals that may share the hospital areas.

HAZARDS TO HUMANS: The larva in the cat is not a hazard to humans. There have been reports, however, of the recovery of larvae of Cuterebra from humans who have become infected in much the same manner as cats (Baird et al., 1989; Schiff, 1993). Most human cases have been reported in the northeastern United States within late August and early September. In humans most larvae have been recovered from the head, neck, shoulders and chest. There have been rare cases of ocular and upper respiratory involvement. It does not appear that central nervous system disease happens in humans as it does in cats.

CONTROL/PREVENTION: Owners could be advised of the life cycle, but it would be difficult to prevent a cat with a desire to hunt from visiting potential sites of egg deposition. Thus, it is important to make owners in areas where the neurologic disease occurs to be aware that the signs of respiratory infection in late summer and early fall would warrant a veterinary consultation and the potential need for careful monitoring.


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Figure 5-57. Adult Cuterebra sp. Typically, the living fly holds its wings along the body when at rest.

Figure 5-58. Third-stage larva of a Cuterebra sp. removed from a cat. This larva is about 3 cm in length.

Figure 5-59. Spiracles on the posterior of the mature Cuterebra sp. removed from a cat.

Figure 5-60. Spines on the body of a third-stage larva of Cuterebra recovered from a rabbit. They are conical with single points.

Figure 5-61 Second instar larva surgically removed from a subcutaneous lesion on a cat.

Figure 5-62. Spiracles of a second-instar larval Cuterebra recovered from a cat.

Figure 5-63. Diagram of the life cycle and pathology caused by Cuterebra spp. in cats. The adult female fly lays its eggs on grass, plant stems, bark, or wood chips around the entrance to a rodent burrow. After several days, the larvae have matured and hatch from the eggshell in response to increases in temperature; some larvae can persist within the eggs for months. The hatched larvae attach to a passing host and then enter the body of the host through a opening such as the mouth or nose. In the rodent and rabbit hosts, the larvae migrate first to areas associated with the lungs or pharynx, and then migrate to the subcutaneous site where the larva matures within the warble. Once the larva has matured, it drops to the ground where it wriggles into the soil to pupate. Typically, the pupal stage is the stage in which the fly overwinters, with the adults emerging from the pupal case in the spring. The most common presentation in the cat is to have the larvae developing in a warble much like they do in the rodent or rabbit with the posterior end of the bot with its large paired spiracles protruding from the opening in the warble. In the cat, neurologic manifestations of infection can be caused by early stage larvae migrating into the spinal cord or brain and amy produce lesions similar to those seen in feline ischemic encephalopathy with appreciable asymmetry of the cerebral hemispheres.

Figure 5-64. The major life stages of Cuterebracuniculi.

Figure 5-65. A warble in the back of a cat with a mature third-instar larva.

Figure 5-66. The larva removed the warble in the back of the cat in Figure 8.

Figure 5-67. Exposed larva within a cat that was euthanatized with severe neurologic signs. [Photo courtesy of Dr. A de Lahunta]

Figure 5-68. The spinal cord of a cat showing a Cuterebra sp.

Figure 5-69. A histological section of a spinal cord of a cat showing the aposition of the Cuterebra larva to the cord material. The larva can be recognized by the large black triangles which represent sections through the large body spines presnet on the developing bot's surface.