Results and discussion

The infectivity of Z. lunata in Balb/c mice from 11 to 24 weeks PI was 6 of 11 (55%), as shown in table 1. Twelve (5%) worms were recovered from the 220 cysts fed to the mice. All worms were found in the caecum and none was in the large intestine. All worms were ovigerous and contained more than 300 eggs per worm. Some eggs released into Locke's solution from a 24-week-old worm were placed in artificial spring water and incubated for 2 weeks at 28°C. These eggs contained fully developed miracidia, indicating that 6-month-old worms were capable of producing viable eggs. Mean body area measurements of worms at 11 weeks PI were about 20 mm² and increased to about 25 mm² by 12 weeks. Worm growth based on mean body area appeared not to occur between 12 and 24 weeks PI (see last column of table 1 for growth data).

Table 1

Host infectivity and worm recovery of 11 adult male Balb/c mice each exposed to 20 Z. lunata cysts and necropsied 11–24 weeks postinfection (PI).

^a From 2 to 4 worms measured at each week PI.

Low infectivity of Z. lunata in the Balb/c mouse is puzzling, as discussed in LeSage & Fried (Reference LeSage and Fried2010). The main finding of our study is that this parasite is able to survive for at least 6 months in the Balb/c mouse and still produce viable eggs. Thus, this model is suitable for studies on ageing and longevity of a digenean in a murine host.

Information summarized by Sandground (Reference Sandground1936) provides the following longevity data for various economically and medically important digeneans. Clonorchis sinensis can survive for more than 25 years in humans and for about 2.5 years in dogs. Fasciola hepatica can survive in cattle and sheep for about 5 years and in experimentally infected rabbits for more than 3 years. The lung fluke Paragonimus kellicoti can survive in humans and felines for 6 years. The human schistosomes are particularly long lived, with reports of Schistosoma haematobium surviving in humans for between 25 and 28 years, and S. mansoni for 20 years. Some information on S. japonicum from animal studies indicates that this digenean survives for about 2 years in experimentally infected horses.

We note below a number of selected studies published after Sandground (Reference Sandground1936) on the topic of longevity of adult digeneans from 1949 to 2008. These studies are listed chronologically rather than by trematode species.

Wallerstein (1949) reported a case of a Puerto Rican woman in New York City who had been out of an endemic schistosome area for more than 26 years; she showed evidence of live adults of S. mansoni in her body. Wallerstein (1949) also noted that similar cases of schistosome longevity had been reported previously for both S. haematobium and S. japonicum, but this was the first report of such long-term survival of S. mansoni in a human. Attwood & Chou (Reference Attwood and Chou1978) reported the persistence a Clonorchis sinensis infection for at least 26 years in the bile duct of a Chinese immigrant in Australia. This digenean, which is a known carcinogen in humans, had not induced neoplasia in the bile duct of the patient. Harris et al. (Reference Harris, Russell and Charters1984) reviewed cases of schistosomiasis in immigrants in Western Australia, and demonstrated the unusual longevity of S. mansoni. They indicated that these worms could survive at least 3 years in humans in imported cases of schistosomiasis. Vercruysse et al. (Reference Vercruysse, Rollinson, van Heerden and Southgate2003) showed that Schistosoma curassoni, a schistosome of sheep, cattle and goats in West Africa, will live for at least 8 years in a sheep. The sheep, which had previously been exposed to cercariae of this schistosome, died of natural causes and at post-mortem adult pairs of S. curassoni were recovered from the mesenteric and rectal veins. This study provides the first record of schistosome longevity based on actual worm counts. Payet et al. (Reference Payet, Chaumentin, Boyer, Amaranto, Lemonon-Meric and Lucht2006) reported a case of S. mansoni infection in an HIV patient 38 years after the individual had left an area endemic for schistosomiasis. Diagnosis was based on the finding of a viable S. mansoni egg following liver biopsy. The patient was treated successfully with a single dose of praziquantel. The final study mentioned in this research note is that of Fried & Peoples (Reference Fried and Peoples2008), who reported the recovery of live, gravid worms of Echinostoma caproni at 23 weeks PI in Balb/c mice. It was this study that suggested the use of the Balb/c mouse as a suitable host to study the effects of long-term survival on the host–parasite relationships of Z. lunata and mice.