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Observations on the Role of Mollusks and Planarians Infection to Man In Rev. Biol. Trop., 24(1): 163-174, 1976 Observations on the role of mollusks and planarians in the transmission of Angiostrongylus cantonensis infection to man in new caledonia * by Lawrence R. Ash** (Received for publication April 9, 1976) Abstract: Observations from October 1965 to May 1967, on the role played by mollusks and other invertebrates in the tr ansmission of Angiostronf{ylus cantonensis infection to man on the South Pacific island of New Caledonia revealed that various snails, slugs and a planarian, ocurring in gardens supplying considerable amounts of edible greenvegetation to local markets, were commonly infected with third-stage larvae of A. cantonensis. The veronicellid slugs, Va ginulus plebeius and Laevicaulus alte, were the most frequently and intensively infected mollusks and they probably serve as the chief reservoir of infection for feral rats. The high level of infection in these slugs not only results in maintaining a largc population of infected rats but is of importance in the dispersal of infective larvae into planarians serving as paratenic hosts for the parasite. There is no apparent seasonal diference in the rate and level of infection among the slugs, although they have a dormant period during the cooler months (July to September) of the year. lt is suggested that planarians are probably the single most important source of human infection in New Caledonia. The planarians show a marked seasonal occurrence, reaching their peak during the cool months of the year, which corresponds to the peak vegetable growing season. Their highly carnivorous habits in their attacking of both snails and slugs results in a high level of infection although individual planarians harbor relatively low numbers of larvae, usually less than 10. Their small size, their ability to fragment easily, and their rapid dehydration to form inconspicuous black masses contaminating lettuce and other vegetables make them an ideal vehicle for the transmission of A. can tonensis to mano Since the discovery in the early 1960's that Angiostrongylus can tonensis, the rat lungworm, is the primary agent causing human eosinophilic meningitis or eosinophilic meningoencephalitis in many islands of the Pacific an d in many countries of Southeast Asia there ha ve be en numerous investigations into the * This study was done while the author was Medical Parasitologist, NIAID, NIH, USPHS, seconded to the South Pacific Commission. ** Division of Epidemiology, School of Public Health, University of California, LosAngeles, California 90024, U.S.A. 163 164 REVISTA DE BIOLOGIA TROPICAL epidemiology of the disease. Most of these studies have cIearIy demonstrated that the manner in which the disease is acquired is related to the preferential food habits of the particular population involved (Rosen et a!., 1961; Alicata, 1963 ; Rosen et al. , 1967; Punyagupta et al., 1970; Vii et al. , 1975). This correlation of disease ocurrence and food habits reflects the numerous opportunities for human infection presented by the wide range of molIuscan intermediate hosts and the numerous invertebrate and vertebrate animals that can serve as paratenic hosts for the parasite. Infective-stage larvae have been found in many molIusks (Wallace and Rosen, 1969a, 1969b), as weIl as in land planarians (Alicata, 1962,1963), shrimp and crabs (Rosen et al. , 1967; Alicata , 1965; Wallace and Rosen, 1966), fish (Wallace and Rosen, 1967), amphibians and reptiles (Ash, 1968), and mammals (Alicata, 1964). Despite the numerous opportunities for human infection presented by readily available intermediate and paratenic hosts other factors appear to be of importance in the occurrence of the disease. Studies in Thailand (Punyagupta et al. , 1970) and in Taiwan (Vii et al. , 1975) have demonstrated the influence of cIimate on the distribution of the disease in time. Prior to these latter two studies Rosen and his colIeagues (Rosen et al. , 1967) had noted a marked seasonal occurrence of the disease on the South Pacific island of New Caledonia. Since initial observations by these workers and others (Alicata, 1963) had indicated a correlation between cases of the disease and the peak vegetable growing sea son on the island, a study was designed to investigate the epidemiologic factors involved in transmission of the disease. A survey of the market gardens supplying significant quantities of produce to markets in the capital city, Noumea, was undertaken from late 1965 to mid-1967 . This report presents data from these gardens on the moIluscan and planarian populations, the factors influencing the size of these populations, the rate and intensity of infection by A. can tonensis in these invertebrates and how alI these factors interrelate to aIlow for transmission of this infection to man. MATERIAL AND METHODS The market gardens selected for study were in the immediate vicinity of the capital city, Noumea, and were the major suppliers of produce to the local markets. These gardens were scattered on the outskirts of diffe rent sections of the city. AlI gardens were bordered on two or more sides by thick brush and vegetation. In cIose association with each garden were either smaIl storage sheds or poultry-raising pens that provided excelIent shelter for rats that were abundant in all gardens.· Although various vegetables were grown in the gardens, the dominant crops were the green salad vegetables, incIuding several varieties of lettuce and cabbage . The growing season for these started in March or April and finished toward the end of the year. During the hot summer months of December to February the bulk of the lettuce consumed by the local population was imported from Australia. The methods used for sampling the molIuscan and planarian populations varied depending upon their abundance. Since slugs and planarians are mainly nocturnal in their habits most collections were made at night. CoIlections were made several times each week for the period spanning October, 1965 to April, 1967. When moIlusks were especially abundant, usually during and foIlowing rainy periods, small and large slugs were collected from aIl parts of the gardens themselves as well as in the brush immediately bordering the gardens. In the hot summer ASH: Angiostrongyius can tonensis in New Caledonia 165 months (December-February) there was a marked reduction in slugs so that all collected were examined. Planarians were found only in the cooler months (June-September) and all collected were examined. Two methods were used for examining mollusks and planarians. Small snails and slugs were examined by press preparations of the entire animal between thick glass plates under a dissecting microscope. Large snails and slugs were subjected to pepsin digestion by techniques previously described (Wallace and Rosen, 19b9c). The veronicellid slugs were weighed and measured individually prior to their examination; however, very young veronice11ids (less than 2 cm in length) were often pooled in groups of 3 to 5 for digestion. When nematode larvae were found they were examined with a compound microscope for morphologic features characteristic for A. eantonensis and other lungworm larvae (Ash, 1970). In sorne instances larvae were fed to white rats and the developing adult worms were searched for in the meninges of these animals 3 weeks later. RESULTS Species of animals present in gardens: The predominant species of rat occurring in association with a11 gardens was Rattus norvegieus; R. rattus was present in fewer numbers. No attempt was made to continuously survey rats for infection with A. eanton ensis. During the first year approximately 70% of 45 R. norvegieus trapped around the gardens studied were infected but only one of 9 R. rattus was infected. Although cats and dogs were owned by most gardeners there was little evidence of their frequent defecation in gardens. Lungworms were never found in dogs but cats were infected with two metastrongylid species, Aelurostrongylus abstrusus and Anafilaroides rostratus. Hookworms and ascarids were the only other intestinal nematodes cornmonlyfound in dogs and cats. Three species each of slugs and snails and one species of planarian were found in the market gardens studied. The slugs included two veronicellid species, Laevieaulus alte (Férussac, 1823) Hoffmann, 1929 and Va ginulus (Sarasinula) plebeius (Fischer, 1868) Baker, 1931, and the small black slug, Deroeeras laeve (Müller, 1774). The three snails found were He!ix (Cryptomphalus) aspersa (Müller, 1774), Bradybaena similaris (Férussac, 1821) and Su bu!ina oetona (Bruguiere, 1792). The only land planarian species occurring in the gardens was Geoplana fo rsterorum Schroder, 1924. Habits of molluks and planarians: The large veronicellid slugs, L. alte and V plebeius, live for the most part in the brush bordering the gardens. They remain under cover during the day and at dark migrate into the gardens wheie they feed primarily on vegetation lying on the ground in and between the planted rows of lettuce and other produce. Once these slugs atta in a length of more than 2-3 cm they feed almost exclusively on vegetation on the ground whereas the young, small slugs may also climb the plants to fe ed on the leaves. These slugs are seasonal ; during the cool months of the year (J uly to September) the adult slugs burrow underground or under vegetation and do not feed on the surface of the ground. Eggs hatch toward the end of the year and tiny veronicellids are the dominan t population during December an d January ; they grow rapidly, attaining lengths of 3-7 cm within a few months and may travel considerable distan ces to feed before returning to the periphery of the gardens. Heavy rainfall, resulting in extremely 166 REVISTA DE BIOLOGIA TROPICAL muddy conditions, discouraged their activity although with normal rainfall they thrived. In the absence of rainfall for extended periods of time, during the warm months of the year, the slugs would remain active unless windy conditions prevailed; wind apparently caused rapid drying of the slugs and was detrimental to their activity and survival.
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