Ancylostomabraziliense de Faria, 1910
ETYMOLOGY:Ancylo = curved + stoma = mouth; braziliense for the geographical location where the worms were first found.
HISTORY: This worm was described in 1910 by Dr. Gomes de Faria from specimens recovered from the intestines of cats and dogs. It was later decided that this species was synonymous with Ancylostomaceylanicum which had been found in cats, dogs, and people in Asia (Lane, 1922; Leiper, 1913). Biocca (1951) redescribed both species and presented convincing evidence that the species were different. Similarly, Beaver (1956) discussed the fact that there had been no confirmed human infections with Ancylostomabraziliense in the United States where it was the only one of these two species present. More recently Rep et al. (1968) and Rep (1972) have further proven that these are separate species by performing single-sex cross-over experiments in dogs. However, there is a period of about 50 years when the majority of workers thought that these were identical forms; thus, it is difficult to examine earlier reports relative to the geographical distribution of these two parasites.
GEOGRAPHIC DISTRIBUTION: It would appear that Ancylostomabraziliense represents an American or African form of the Ancylostomaceylanicum hookworm of Asia. Biocca (1951) only identified specimens of Ancylostomabraziliense from Africa and South America. This worm has also been reported from Central and North America. Yoshida et al. (1974) reported that it appears in Japan, and there have been additional reports of mixed infections in cats with Ancylostomabraziliense and Ancylostomaceylanicum in Indonesia (Soeripto et al., 1978) and Malaysia (Amin-Babjee, 1978; Yoshida et al., 1973). Ancylostomabraziliense appears to prefer coastal areas, at least in the Americas, hence the prevalence of this parasite tends to drop as one moves inland. It is possible that Ancylostomabraziense has higher requirements for sandy conditions or can withstand more readily the higher levels of salt found in coastal soils.
LOCATION IN HOST: The adults are found within the anterior small intestine of the feline host. It appears that larvae are capable of persisting in the tissues of the feline host, but this has not been examined in any detail.
PARASITE IDENTIFICATION: The adults of Ancylostomabraziliense are 4 to 10.5 mm long. Members of the genus Ancylostoma can be distinguished from Uncinaria by determining whether or not there are ventral teeth in the buccal capsule. Specimens of Ancylstoma have large teeth within the buccal capsule while specimens of Uncinaria are recognized by the presence of cutting plates. The adults of Ancylostomabrazilinese and Ancylostomaceylanicum possess only two teeth on the ventral aspect of the buccal cavity with the lateral tooth being large and the median tooth quite small. The adults of Ancylostomatubaeforme have three teeth on each side of the buccal capsule. Ancylostomabraziliense can be differentiated from Ancylostomaceylanicum by careful examination of the teeth within the buccal cavity. The medial teeth are smaller in Ancylostomabraziliense then they are in Ancylostomaceylanicum. Another means of separating these two species is by careful examination of the copulatory bursa of the male. The lateral lobes of the bursa are relatively shorter in Ancylostomaceylanicum than they are in Ancylostomabraziliense and the branching of the externo-dorsal rays occurs more posteriad in Ancylostomaceylanicum than it does in Ancylostomabrasiliense. Finally, Yoshida (1971a) showed that if the adults are killed in hot water (149F or 65 C) prior to fixation that about 90% of the females of Ancylostomabraziliense are noted to have a distinct 20 degree bend in the body at the level of the vulva (about two-thirds back on the body from the anterior end). This bend does not occur with Ancylostomaceylanicum adults.
The eggs of the different Ancylostoma species found in the cat are apparently indistinguishable from each other. The eggs of Ancylostomabraziliense are considered by most workers (e.g., Sarles, 1929) to be slightly smaller (55 m x 34 m) than those of Ancylostomacaninum (62 m x 38 m). The eggs of Uncinaria are considered larger than those of Ancylostoma being 70 to 90 m long by 40 to 50 m wide. The two eggs are easy to distinguish in mixed infections (Ehrenford, 1953).
Yoshida (1971b) showed that the infective-stage larvae of Ancylostomabrazilinese average 662 m in length, which made them recognizably shorter than the larvae of Ancylostomaceylanicum which averaged 712 m in length. The larvae of Ancylostomabraziliense are thus slightly longer than the larvae of Ancylostomacaninum which average 630 m in length (Lucker, 1942) and slightly longer than the larvae of Ancylostomatubaeforme that have been reported to be 630 m long (Okoshi and Murata, 1967). The infective-stage larvae of the Ancylostoma species are all longer than the larvae of Uncinariastenocephala which measure only 500 to 580 m in length. Thus, ranking the infective-stage larvae of the four major feline hookworms there is Ancylostomaceylanicum (712 m), Ancylostomabraziliense (660 m), Ancylostomatubaeforme (630 m), and Uncinariastenocephala (<600 m).
LIFE CYCLE: Cats can be infected by the ingestion of larvae or by the larvae penetrating the skin. When cats are infected orally with third-stage larvae, these infective larvae enter the intestine mucosa. Within the mucosa, these larvae develop to the fourth stage. The larvae then appear in the intestinal lumen after the second day of infection. The prepatent period of the infection in cats following oral infection is 14 to 16 days. If cats are infected through the skin, the larvae migrate via the bloodstream to the lungs, migrate up the trachea, and are then swallowed. When the larvae reach the small intestine, most are still young third -stage larvae. The prepatent period following percutaneous infection can be 13 to 27 days (Dove, 1932).
Cats can also be infected by the ingestion of paratenic hosts. In mice after oral or percutaneous infection, the larvae migrate via the bloodstream to the lungs and then proceed to the area of the head of the mouse, where they persist for up to 18 months. In mice, most larvae are found within salivary glands or within the nasopharyngeal epithelium (Norris, 1973). Cats have been experimentally infected by feeding them larvae recovered from infected mice (Norris, 1971).
On the basis of a single trial, it would appear that transplacental and transmammary transmission of Ancylostomabraziliense does not occur in dogs (Miller, 1971). This has not been examined in the cat.
The aults of Ancylostomabraziliense have been reported to live about four to eight months (Sarles, 1929). A single female worm produces between 200 to 6000 eggs per day (Sarles, 1929). As the infection matures, the number of eggs produced by a single female will decline. The infection of younger cats can be more easily obtained than the infection of older cats (Sarles, 1923).
CLINICAL PRESENTATION AND PATHOGENESIS: When Ancylostomabraziliense was orignally described, it was noted that this hookworm was not as pathogenic as Ancylostomacaninum (Gomes de Faria, 1910). Very little hemorrhage occurs at the site of larval development or adult attachment. Using 51Chromiaum-labelled erythrocytes, it has been shown that the blood loss due to infections of adult worms in kittens is about 1 to 2 ul of blood/worm/day (Miller, 1966). Blood loss was first detected in cats 10 days after infection, and the experimentally infected kittens maintained hemoglobin levels, hematocrit values, and weight gains that were comparable to uninfected age-matched control kittens.
TREATMENT: Products approved for the treatment of Ancylostomabraziliense by oral administration include (Bowman, 1992): toluene (in a dichlorophen-toluene mixture with a dose of 264.5 mg toluene per kilogram body weight), dichlorvos (11.1 mg/kg), febantel (as a febantel-proaziquantel mixture; 10 mg/kg BW febantel for adult cats and 15 mg/kg BW febantel for kittens), and n-Butyl chloride (400 mg/kg). Ivermectin as a chewable product (administered at 24 g/kg) that is to be administered monthly is reported to reduce infections by 98.1% as compared to untreated controls (Nolan et al., 1992). Disophenol sodium is approved at 10 mg/kg in a formulation that is to be administered subcutaneously.
EPIZOOTIOLOGY:Ancylostomabraziliense is a parasite that is most commonly found in coastal areas with sandy soils. The development of the infective-stage larva has been shown to undergo optimal development at 27C (Rep, 1965). There has been little examination of the effects of salinity on the development of the infective larvae of this hookworm, but one would suspect that the larvae can develop in rather high salt concentrations. It is also likely that these worms do not develop well in areas where there are freezing temperatures that occur for extended periods.
HAZARD TO OTHER ANIMALS:Ancylostomabraziliense is a parasite that is capable of infecting dogs as well as cats. It is also highly likely that if the conditions are appropriate for the development of the larvae, that tey could infect small mammals that share ground with the infected cat. There has been almost no attention given to the actual disease caused in rodent hosts.
HAZARD TO HUMANS:Ancylostomabraziliense is probably the major cause of human cases of cutaneous larva migrans. That this was the major cause of hookworm induced cutaneous larva migrans in the United states was shown clearly by Dove (1932). Cases of cutaneous larva migrans continue to be not uncommon, especially in travelers who have visited the Carribean (Davies et al., 1993). Occasionally, cases of creeping eruption are reported from unusual temperate locations (Klose et al., 1996). In some instances, the large numbers of larvae that enter an individual will undergo the initial portion of a somatic migration and cause severe pneumonitis that might require hospitalization (Beaver et al., 1984).
CONTROL/PREVENTION: Cats are being infected by the ingestion of larvae when eating grass or grooming, by larvae penetrating the skin, or the ingestion of larvae in paratenic hosts. Thus, whenever cats are in an endemic area and have access to the outside, they are probably at risk of contracting this infection. The recent availability of a monthly heartworm preventative that is also capable of treating adult hookworm infections will make it possible to protect cats from infections with this parasite.
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