Ancylostoma tubaeforme (Zeder, 1800)
(Figures 4-09 through 4-10)
ETYMOLOGY:Ancylo = curved and stoma = mouth; tubae = straight trumpet and forme = shape. The original spelling of the genus was Agchylostoma due to improper transliteration of the Greek root, and this was later corrected to Ancylostoma.
SYNONYMS:Strongylus tubaeforme, Ancylostoma caninum var. longespiculum.
HISTORY: This worm was originally described as a separate species parasitizing the cat by Zeder in 1800. However, it was later considered as a variety of the dog hookworm, Ancylostoma caninum. It was finally given a firm position as a separate species within the genus by Burrows (1962) who compared the adults of Ancylostomatubaeforme with those of Ancylostomacaninum.
GEOGRAPHIC DISTRIBUTION: This worm is found throughout the world, wherever there are domestic cats (Rep, 1966).
LOCATION IN HOST: The adult worms are found within the small intestine of the feline host. Most adult worms are found within the portion of the jejunum closest to the duodenum.
PARASITE IDENTIFICATION: The adults of Ancylostomatubaeforme are 7 to 12 mm long. If it is necessary to distinguish the adult specimens of hookworms found in the cat, the separations can be made on the basis of the shape of the buccal capsule. First, members of the genus Ancylostoma can be separated from those of 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. They can be differentiated from the adults of Ancylostomabraziliense and Ancylostomaceylanicum by the presence of three teeth on either side of the ventral midline (Ancylostomabrazileinse and Ancylostomaceylanicum each possess two such teeth).
The eggs of the different Ancylostoma species found in the cat are apparently indistinguishable from each other (Fig 4-09). The eggs of Ancylostomatubaeforme have been measured to be 55-76 by 34-45 m with means of 61 by 40 m. The eggs of Uncinaria are 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).
LIFE CYCLE: The life cycle of Ancylostomatubaeforme has been studied in some detail (Okoshi and Murata, 1967 a-d). The optimal temperature for larval develop is 68F (20C), which is lower than the optimal temperature for developing larvae of Ancylostomacaninum. The infective third-stage larvae of Ancylostomatubaeforme can infect cats both orally or through skin penetration.
After oral inoculation, the larvae enter the wall of the stomach and proximal small intestine where they remain for 10 to 12 days while developing to the adult stage. The adults then reenter the lumen. The prepatent period of Ancylostomatubaeforme following oral administration is 18 to 28 days which is longer that the prepatent period of the other cat hookworms. The worms have reached their maximum length about one month after the cat was initially infected.
After larvae penetrate the skin, they migrate through the lungs, up the trachea, and down the esophagus. The larvae then spend very little time within the wall of the gastrointestinal tract. Development of fourth-stage larvae is more rapid in larvae that have penetrated the skin, but there is no apparent growth of the larvae before they reach the intestinal tract. The prepatent period is between 19 to 25 days following skin penetration. Penetration of the skin is likely due to the secretion of proteolytic enzymes, although, an early investigation failed to reveal any when the larvae of Ancylostomatubaeforme were examined (Mathews 1975).
Rodents can serve as paratenic hosts. After both oral and percutaneous infection, larvae are found concentrated in the cranial aspect of their murine host, where they have remained alive for up to 10 months (Norris, 1971). Larvae from mice have been shown to infect other mice where they are capable of again entering the tissues and persisting. There does not appear to have been any attempts to infect cats with larvae from mice.
It is assumed that there is neither transplacental nor transmammary transmission of hookworms from the queen to her kittens. This assumption is consistent with the lack of hookworm disease seen in young kittens and the small number of larvae that have been recovered from the viscera and musculature after being infected with larvae either by the oral or percutaneous route (Okoshi and Murata, 1967d). However, this question has never actually been carefully addressed experimentally.
The life expectancy of the adult worms has been observed to be 18 months to 2 years in experimentally infected cats (Oshida and Murata, 1967c). Cats tend to harbor relatively few adult worms. The examination of cats in New Jersey revealed between 1 tto 123 worms per cat (with a mean of 20) in 235 cats that had adult worms. There has been no examination as to the number of eggs produced by a female each day or the effects of the age of cats on the ability of worms to mature to the adult stage within the intestine.
CLINICAL PRESENTATION AND PATHOGENESIS: The main clinical signs associated with an infection of Ancylostomatubaeforme are weight loss and a regenerative anemia (Onwuliri et al., 1981). When cats were given 1000 to 2000 infective-stage larvae, they lost weight when compared to cats receiving 0, 100 or 500 larvae. The cats that received 1000 or 2000 larvae died, and in these cats, hemoglobin levels fell to 4 g/dl and packed cell volumes fell to 20% after the cats were infected for a month. In the cats receiving fewer larvae, the hemoglobin levels and packed cell volumes also fell, but then the levels seemed to stabilize after six weeks.
The hookworms cause significant blood loss from the intestinal mucosa (Fig 4-10). Cats experimentally infected with Ancylostomatubaeforme can die from the infection. Rohde (1959) gave cats infective larvae, and within 12 to 47 days after the cats were infected, 16 of them died. Examination of the intestines after death revealed that these cats harbored between 7 to 290 adult worms (mean of about 100 worms per cat). Nine Siamese cats given 2000 larvae, and six of nine Siamese cats given 1000 infective-stage larvae died within 46 days of the initiation of the infection. These cats were found to harbor between 183 to 213 adult worms within their samll intestines.
TREATMENT: There are several products marketed for the treatment of Ancylostomatubaeforme in cats. Oral treatments with dichlorvos (11.1 mg/kg body weight), febantel and a febantel-praziquantel mixture (10 mg febantel/kg in cats and 15 mg febantel/kg in kittens), and n-Butyl chlorid (400 mg/kg) are marketed for cats as well as disophenol sodium (10 mg/kg body weight, SQ) (Bowman 1992). Ivermectin is now available as a chewable for cats with an efficacy of 90.7% for treatment of Ancylostoma caninum in cats (Nolan et al., 1992).
EPIZOOTIOLOGY: It is highly likely that cats become infected both by the ingestion of larvae, larvae penetrating the skin, or the ingestion of infected rodent paratenic hosts. Thus, there is every reason to believe that cats become infected while eating grass, ingesting larvae hile grooming, or by larvae penetrating the skin of cats waling on infected soils. Also, cats that hunt would have a greater likelihood of becoming infected.
HAZARD TO OTHER ANIMALS: Mice and other rodents can become infected with the larval stages of this hookworm. It would appear that Ancylostomatubaeforme does not develop to the adult stage in any hosts except felines.
HAZARD TO HUMANS: Adult Ancylostomatubaeforme have not been recovered form humans. Also, it would appear that Ancylostomatubaeforme is not a major cause of cutaneous larva migrans since it appears that this occurs mainly in geographical areas where Ancylostomabraziliense is prevalent.
CONTROL/PREVENTION: If cats have access to the outside, prevention will be difficult. The marketing of a new monthly product with efficacy against this hookworm will provide control of this parasite in cats placed on this program.
Burrows RB. 1962. Comparative morpholoogy of Ancylostomatubaeforme (Zeder, 1800) and Ancylostomacaninum (Ercolani, 1859). J Parasitol 48:715-718.
Ehrenford FA. 1953. Differentiation of the ova of Ancylostomacaninum and Uncinariastenocephala in dogs. Am J Vet Res 14:578-580.
Mathews BE. 1975. Mechanism of skin penetration by Ancylostomatubaeforme larvae. Parasitology 70:25-38.
Nolan TJ, Niamatali S, Bhopale V, Longhofer SL, Schad GA. 1992. Efficacy of a chewable formulation of ivermectin against a mixed infection of Ancylostomabraziliense and Ancylostomatubaeforme in cats. Am J Vet Res 53: 1411-1413
Norris DE. 1971. The migratory behavior of the infective-stage larvae of Ancylostomabraziliense and Ancylostomatubaeforme in rodent paratenic hosts. J Parasitol 57:998-1009.
Okoshi S, Murata Y. 1967a. Experimental studies on ancylostomiasis in cats. II. Morphology of the eggs and larvae of Ancylostomatubaeforme Zeder, 1800 and Ancylostomacaninum Ercolani, 1859. Jap J Vet Sci 29:133-140.
Okoshi S, Murata Y. 1967b. Experimental studies on ancylostomiasis in cats. III. Egg culture of Ancylostomatubaeforme Zeder, 1800 and Ancylostomacaninum Ercolani, 1859. Jap J Vet Sci 29:174-177.
Okoshi S, Murata Y. 1967c. Experimental studies on ancylostomiasis in cats. IV. Experimental infection of Ancylostomatubaeforme and Ancylostomacaninum in cat. Jap J Vet Sci 29:251-258.
Okoshi S, Murata Y. 1967d. Experimental studies on ancylostomiasis in cats. V. Visceral migration of larvae of Ancylostomatubaeforme and A.caninum in cats. Jap J Vet Sci 29:315-327.
Onwuliri COE, Nwosu ABC, Anya AO. 1981. Experimental Ancylostomatubaeforme infection of cats: changes in blood values and worm burden in relation to single infections of varying size. Ztsch Parasitenk 64:149-155.
Rep BH. 1966. On the polyxenia of Ancylostomidae and the validity of the characters used for their differentiation. II. Trop Geogr Med 12:271-326.
Rhode K. 1959. Vergleichende Untersuchungen über die Hakenwürmer des Hundes und der Katze un Betrachtungen über ihre Phylogenie. Ztsch Tropenmed Parasitol 10:402-426.
Zeder JGH. 1800. Erster Nachtrag sur Narugeschichte der Eingeweidewürmer, mit Zusätzen un Anmerkungen herausgegeben. Leipzig.
Figure 4-09. Ancylostoma tubaeforme: Eggs of this hookworm as they are passed in the feces of the feline host.
Figure 4-10.Ancylostoma tubaeforme: Intestine of a cat that had been infected with approximately 100 adult hookworms. Note the amount of free blood within the intestinal lumen.