Ancylostoma ceylanicum (Looss, 1911)
ETYMOLOGY: Ancylo = curved and stoma = mouth; ceylanicum for the location from where the host containing these parasites was originally obtained.
SYNONYMS:Agchylostoma ceylanicum, Ancylostoma gilsoni
HISTORY:Ancylostoma ceylanicum, like Ancylostoma tubaeforme, was originally described as a separate species parasitic in the cat and then considered for a period as a synonym of a canine parasite, I WANT TO CHANGE THIS in this case Ancylostomabraziliense. Looss (1911) described Ancylostomaceylanicum based on specimens recovered from a civet cat in Ceylon. A couple of years later, three human prisoners in India were found to have hookworms that were identified as Ancylostoma ceylanicum by Lane (1913). However, others felt that Ancylostoma ceylanicum should be considered identical to Ancylostoma braziliense (Lane, 1922; Leiper, 1913). It was in 1951 that the redescription of Biocca established the criteria upon which this species can be separated from Ancylostoma braziliense. Rep et al. (1968) and Rep (1972) performed single sex crossover experiments between males and females of Ancylostoma ceylanicum and Ancylostoma braziliense in dogs and found that fertilized eggs were produced only when both sets of worms represented the same species.
GEOGRAPHIC DISTRIBUTION: During the first half of the twentieth century, when Ancylostomaceylanicum was considered a synonym of Ancylostoma braziliense, distinctions were not drawn between the two in different surveys. However, after 1951, most reports have dealt with the two species separately. Ancylostomaceylanicum is a parasite capable of developing to the adult stage in humans and hamsters, while Ancylostoma braziliense remains restricted to feline and canine hosts. Thus, earlier surveys of humans where infections were identified as being caused by Ancylostomabraziliense probably represent infections with Ancylostomaceylanicum (Beaver , 1956). The distribution of Ancylostomaceylanicum seems to extend south from India (Chowdhury and Schad, 1972; Ray et al., 1972) down the eastern coast of Africa to Madagascar and South Africa (Baker et al., 1989; Yoshida, 1971; Yoshida et al., 1973). The range also extends east from India into Indonesia, Singapore, Malaysia, and Thailand (Amin-Babjee, 1978; Rohde, 1962; Setasuban et al., 1976; Soeripto et al., 1978; Yoshida, 1971; Yoshida et al., 1973). Ancylostomaceylanicum has also been reported from some pacific islands, including Taiwan and Okinawa (Yokogawa and Hsieh, 1961), Philippines (Arambulo et al., 1970), Sri Lanka (Dissanaike, 1961), British Solomon Islands (Haydon and Bearup, 1963), Fiji (Yoshida, 1971a), and Japan (Yoshida and Okamoto, 1972).
LOCATION IN HOST: Adults of Ancylostomaceylanicum are found within the small intestine of the cat with the majority being found within the jejunum (Baker et al., 1989). After the oral incoulation of larvae, the worms remain within the intestinal tract; if a dog is infected by skin penetration, the worms migrate through the lungs before entering the intestinal tract. It is not known if there are any arrested stages in the tissues of cats as there would be with Ancylostomacaninum in the dog or to a smaller extent with Ancylostomatubaeforme in the cat..
PARASITE IDENTIFICATION: The adults of Ancylostomaceylanicum are 6 to 10 mm long and appear to be slightly stouter than the adults of Ancylostomabraziliense. 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. Like Ancylostomabraziliense, the adults of 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 will have three teeth on each side of the buccal capsule. Ancylostomaceylanicum can be differentiated from Ancylostomabraziliense by careful examination of the teeth within the buccal cavity. The medial teeth are larger in Ancylostomaceylanicum than they are in Ancylostomabraziliense. 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 Ancylostoma braziliense and the branching of the externo-dorsal rays occurs more posteriad in Ancylostomaceylanicum than it does in Ancylostomabrasiliense. Ancylostomaceylanicum has transverse striations in the cuticle that occur about 4 m to 5 m apart while the similar striae in Ancylostoma braziliense are about 8 m to 9m apart.
The eggs of the different Ancylostoma species found in the cat are apparently indistinguishable from each other. The eggs of Ancylostomaceylanicum have been measured to be 60 m by 2 m (Arambulo, et al., 1970). 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 representative of these different genera are easy to distinguish in mixed infections (Ehrenford, 1953).
Yoshida (1971b) showed that the infective-stage larvae of Ancylostomaceylanicum which measured 712 m in length were significantly longer (712 m) than the larvae of Ancylostomabraziliense which measure 662 m in length. Also, Yoshida demonstrated that the distance from the tip of the tail of the infective-stage larva to the end of the sheath was greater in Ancylostomaceylanicum than it was in Ancylostomabraziliense. The larvae of Ancylostomaceylanicum were similar in length to the larvae of Ancylostoma duodenenale, the human species of Ancylostoma. Kumar and Pritchard (1992) showed that lectins could be used to distinguish between the larvae of Ancylostomaceylanicum and Ancylostomaduodenale.
LIFE CYCLE: The life cycle has been examined by Yoshida (1971 a&b) and Yoshida et al. (1974). Work was presented following both oral infection of puppies and afer cutaneous infection. In the case of oral infection, the third-stage larvae molted in the intestinal wall two to three days after infection. The fourth-stage larvae entered the lumen and immature adult hookworms were recovered beginning the sixth day after infection. In these puppies the prepatent period was 14 days. When puppies were infected by allowing larvae to penetrate the skin, the larvae underwent a lung migration, and molted to the fourth-stage in the trachea and stomach. Following skin penetration, many larvae are associated with the hair-follicle system and most of the larvae were found in the skin 6 hours after larvaal application (Vetter and Leegwater-Linden., 1977). Fourth-stage larvae were recovered three days after infection, and adults were recoved beginning seven days after the puppies were infected. The prepatent period was the same as in oral infection. The number of worms recovered following oral infection was 90%, but only 15% of the worms that infected via skin penetration were recovered. Yoshida (1968) reported the prepatent period in cats to be 14 to 17 days. Puppies excreted eggs in their feces for 36 weeks after infection, which is when this study was terminated (Carrol and Grove, 1984).
An examination of dogs that were challenged with additional infective-stage larvae after their previous infection had been cleared by anthelmintic medication (pyrantel pamoate and bunamidine hydrochloride) indicated that there is some resistance to secondary infection (Carroll and Grove, 1985). When the dogs were reinfected a month after the clearing of the primary infection, the adult worm burdens were reduced 77% compared to control dogs infected at the same time. Thus, for at least a month after the clearance of the primary infection, there appears to be some resistance to additional infection. In a second set of experiments, dogs were given a superimposed infection four weeks after the primary infection was induced (Carroll and Grove, 1986). Thus, dogs received 500 larvae and no challenge, 500 larvae and a challenge of 5000 larvae, or only the 5000 challenge larvae. In this experiment, the number of eggs produced by the dogs receiving 500 larvae remained the same throughout the trial, while the number of eggs produced by the group receiving only 5000 larvae were much higher. The number of worms recovered from the superinfectd group (the group receiving 500 and then an additional 5000 larvae) was reduced 78% below that of the dogs receiving only the 500 challenge larvae. The dogs receiving 5000 larvae developed anemia while the other dogs did not.
Mice can serve as paratenic hosts, but it would seem that the percentage of larvae persisting in the mice is quite small. Fukutome (1975) found only 0.1% of the original inoculum present in the muscles of the infected mice. Ray and Bhopale (1972) succeeded in infecting hamsters with the adults of Ancylostomaceylanicum.
CLINICAL PRESENTATION AND PATHOGENESIS: As with other hookworms, the major presentation of an infected animal is regenerative anemia. Areekul et al. (1975) examined the amount of blood loss in experimentally infected dogs using 51Cr labelled red cells. They found that blood was first detected in the feces 10 to 13 days after cutaneous and 8 to 16 days after oral infection. The mean blood loss was found to be around 0.035 ml per worm per day. When dogs were given 12,150 larvae, they developed bloody diarrhea and iron-deficient anemia (Carroll and Grove, 1984). When dogs were given 2000 infective-stage larvae and monitored over a 36 week period, they developed normocytic anemia and eosinophilia. Dogs with severe microcytic anemia show greater autohemolysis of the blood cells when in the presence of glucose (Carroll et al., 1984). There are no appreciable clinical signs in either experimentally or naturally infected cats.
An examination of the feeding sites of Ancylostomaceylanicum in dogs reveals that the heads are deeply buried in the mucosa of the wall of the small intestine (Carroll et al., 1985). Atrophy and villus ulceration surrounding the attachment sites. Large numbers of erythrocytes are found surrounding sites where worms have detached. Around the heads of the worms there is an infiltation of neutrophils, eosinophils, and plasma cells (Carroll et al., 1984). Erythrocytes were found extravascularly within the lamina propria and the mucosa within the buccal capsules of the worms was in varying stage of lysis. The mucosa around the head of the worm was ulcerated and surrounding enterocytes were small and displayed a loss of microvilli.
TREATMENT: There appear to be no reports of treatment of infected cats. Infections in dogs can be cleared using pyrantel pamoate and bunamidine hydrochloride (Carroll and Grove, 1985). Work in experimentally infected hamsters has indicated that the worms appear sensitive to mebendazole, but relatively refractory to thiabendazole (Misra et al., 1981); however thiabendazole can be efficacious in hamsters when used at 200 mg/kg body weight (Kamath et al., 1985). Oxfendazole (20 mg/kg body weight ) has also proven highly efficacious in the hamster (Bhopale et al., 1984). Ivermectin at 100 g/kg body weight was 100% efficacious in experimentally infected hamsters., and pyrantel pamoate was 100% efficacious when given at 100 mg/kg. Children infected with Ancylostoma ceylanicum have been successfully treated with mebendazole (Nontasut et al., 1987).
EPIZOOTIOLOGY: There is very little information available on the development of the larvae of Ancylostomaceylanicum from the egg to the infective stage larva. Yoshida et al. (1974) found that larvae were more likely to develop to the adult stage after oral inoculation than after skin penetration.
HAZARD TO OTHER ANIMALS: Dogs are routinely infected with this parasite. Thus, if dogs and cats are sharing the same pens or yards, there is a good chance that both hosts will be infected.
HAZARD TO HUMANS: Humanscan serve as hosts to Ancylostomaceylanicum. The larvae are capable of penetrating the skin and cause papular eruptions at the sites of larval penetration (Widjers and Smit, 1966). The prepatent period in humans is 18 to 26 days (Bearup, 1967; Yoshida, et al., 1972). Thus, in areas where this hookworm is found, it is of extra importance that cats be kept free from infection. It is also important that the staff of animal hospitals be made aware of the cross transmission capabilities of this parasite.
CONTROL/PREVENTION:Ancylostomaceylanicum has the broadest host range of any of the hookworms infecting the cat. The worms can survive in dogs and humans, as well as in the feline host. Thus, it is important that the control of this parasite include routine examinations and treatments of cats if necessary.
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