International Journal for Parasitology 28 (1998) 607-610

RESEARCH NOTE

First report of the isolation of an adult worm of the genus Brachylaima (Digenea: Brachylaimidae), from the

gastrointestinal tract of a human Andrew R. Butcher,“* Paramaswaami Parasuramar,b Cherie S. Tbmpson”

and David I. GroveC “Infkctious Diseases Laboratories, Institute of Medical and Veterinary Science, Frame Rood, Adelaide, SA, Australia

b14 South Terrace, Kapunda, SA, Australia ‘Department of Clinical Microbiology and Infectious Dkeases, The Queen Elizabeth Hospital, WoodviNe, SA, Australia

Received 5 November 1997; received in revised form 19 December 1997; accepted 19 December 1997

Abstract

A 78-year-old woman presented with an 18-month history of intermittent diarrhoea. Examination of her stools revealed brachylaimid eggs, which were present in three separate specimens over a week. After tre&tm@~t tith prati- quantel a degenerate adult Bruchyluimu species was recovered from her faeces. She lived in a ruts1 area of South Australia and ate vegetables grown in her own garden which had been infested with helicid snails. in South Australia these introduced European helicid snails are commonly infected with brachylaimid intermediate larval stages and are considered to be the source of the human infection. 0 1998 Australian Society for Parasitology. Pub&&d by Elsevier Science Ltd.

Ke.v words: Trematode; Digenea; Brachylaimidae; Brachykaima; Australia; Human, Intestinal fluke infection; H&&i snail

Brachylaimids are trematodes that infect mammals, birds, reptiles and amphibians, with land snails as the first and second intermediate hosts. A review of the literature by Gibson and Bray [I] uncovered 71 species of brachylaimids infecting 338 different animal host species. Brachylaimids can therefore be regarded as a significant family among the digenetic trematodes. Recently, the first human

*Corresponding author. Present address: infectious Disease Laboratories, Institute of Medical and Veterinary Science, PO Box 14 Rundle Mall, Adelaide, SA 5000, Australia. Tel: 08 8222- 3332; Fax: 08 8222-3543; e-mail: andrew.butcher@imvs.sa.gov.au.

infections with a bra&ylaimid were described in two young childn~ in rural SCYW& Australia in

were sea ~~~ in the stools, but IIO t woam wref fbmd [2]. We now describe the worm from the

in stoois is not spsriows, able to complete its life-

cycle in humans. A 78-year-old female da

Hospital in rurzd South an exacerbation of dyspwea due to c&-6& congestive cardiac failure. She was noted to have diarrhoea with offensive stools several times a day. Further

30020-7519/98 $19.00+0.00 0 1998 Australian Society for Parasitology. Published by Elsevier Science Ltd. Printed in Great Britain PII: SOO20-75 19(97)00005-8

608 A.R. Butcher et al. / International Journalfor Parasitology 28 (1998) 607410

enquiry revealed that she had been having inter- mittent episodes of diarrhoea over the preceding 18 months. Two faecal specimens, collected 4 days apart, contained eggs of a brachylaimid trematode similar to those described by Butcher et al. [2]. Five days later the patient was transferred to The Queen Elizabeth Hospital, Adelaide, where further faecal samples showed the same eggs. All bacterial cultures were negative for other patho- gens. A blood film at this time disclosed a blood eosinophil count of 0.90 x 10gL-’ (normal range =0.04-0.4 x 10’ L-l). The patient was treated with praziquantel 600mg orally twice daily for 2 days and all bowel motions were collected for the following 2days. A degenerate gravid adult bra- chylaimid worm (Figs 1 and 2) was recovered from faeces collected on the first day of treatment. Egg clearance occurred by the second day of treatment and stools remained negative for the next 8 months. The patient was discharged from the Queen Eli- zabeth Hospital and returned to the Kapunda Hos- pital, being discharged 1 week later with no further gastrointestinal symptoms. Over the next 8 months

the patient gained 2 kg in weight and had no recur- rence of diarrhoea. Eosinophil counts of peripheral blood were within normal limits.

The diarrhoea began about 18 months before admission to Kapunda Hospital. At that time there was both a mouse plague and a plague of helicid snails in the district. The patient had a vegetable patch in her garden and frequently ate home-grown vegetables. Stools were also obtained from her hus- band and about a dozen relatives who sometimes came to her house for a meal; all were negative for brachylaimid eggs.

The life-cycle of brachylaimid flukes involves the passing of eggs in the faeces of the definitive host; ingestion of these eggs by a suitable land snail; development of a sporocyst in the digestive gland of the snail; release of the first larval stage, cercariae, in the snail’s slime trail; cercariae entering a second intermediate land snail host; development of a cer- caria into a metacercaria in the snail’s kidney; and finally, ingestion of a metacercaria by the definitive host, resulting in the development of an adult worm in the intestinal tract [3].

Fig. 1. Lateral view of a degenerate brachylaimid adult worm recovered from human faeces after treatment with praziquantel. The gravid uterus (u) and the ventral sucker (vs) are present, with all other morphological features being distorted. Scale bar = 500 pm.

A.R. Butcher et al. 1 International Journalfor Parasitology 28 (1998) 607410 609

Fig. 2. Higher powered view of the same degenerate brachylaimid adult worm as in Fig. 1, showing the ventral sucker fvs) and the gravid uterus (u) filled with eggs. Scale bar = 500 pm.

It is postulated that this patient became infected after inadvertently eating snails containing meta- cercariae which were present on home-grown salad vegetables. Alternatively, viable metacercariae may have been deposited on the vegetables via the snail’s slime trail and excreta and/or from the presence of crushed snails.

The snails most likely to be involved are the intro- duced European helicid land snails, which are noxi- ous pests in the district [4]. In South Australia they are known to harbour brachylaimid intermediate stages [5]. The helicid snail Cernuellu virguta is prevalent in the local district and snails collected from the Kapunda district were infected with bra- chylaimid cercariae and metacercariae.

In our original report [2] we described the eggs observed as being those of Brachylaima species, although no adult worm had been seen. We should really have described them merely as eggs of the family Brachylaimidiae, as all brachylaimid eggs are similar in morphology. The worm recovered from this patient was not sufficiently preserved to

permit formal identification. However, we have recently established a life-cycle of this parasite in the laboratory (unpublished observations). Ew from this patient’s faeces were pa through first intermediate snail hosts and the resulting cercariae used to infect second intermediate snail hosts, then Swiss outbred mice were infected with the met- acercariae. Adult fluke worms recovered fern these mice have been identified as belonging to the genus Brachylaima, although precise species i~~~~~ti~n has yet to be determined. We thus canfirm that this human infection is with a fluke worm of the genus Brachylaima.

Kapunda is 130 km from Maitland, where the two original cases were described. Infmtion is likely to be much more widespread in rural South Aus- tralia and perhaps in other parts of this country than has previously been appreciated.

Acknowledgements-We would like to acknowledge the expert opinion of Dr T.H. Cribb, Department of Parasitology, Uni- versity of Queensland, St. Lucia, Australia for confirming the

610 A.R. Butcher et al. / International Journalfor Parasitology 28 (1998) 607610

genus identification of the brachylaimid larval stages and adult worm. Thanks are also extended to the IMVS photographic unit for figure preparation.

References

[l] Gibson DI, Bray RA. The evolutionary expansion and host parasite relationships of the digenea. Int J Parasitol 1994;24:1213-1226.

[2] Butcher AR, Talbot GA, Norton RE, et al. Locally acquired Brachylaima sp. (Digenea: Brachylaimidae) intestinal fluke

infection in two South Australian infants. Med J Aust 1996;164:475-478.

[3] Mas-Coma S, Montoliu I. The life cycle of Brachylaima ruminae n. sp. (Trematoda: Brachylaimidae). a parasite of rodents. Parasitol Res 1986;72:739-753.

[4] Baker GH. The biology and control of white snails (Mol- lusca: Helicidae), introduced pest in Australia. Technical paper. Commonwealth Scientific and Industrial Research Organization, Division of Entomology, Australia, 1986;25:1-33.

[5] Cribb TH. Introduction of a Brachyfaima species (Digenea: Brachylaimidae) to Australia. Int J Parasitol 1990;20:789- 796.