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Tungiasis is a parasitic skin disease caused by the penetration of the female sand flea (Tunga penetrans) into the epidermis of its host. The zoonosis is widespread in resource-poor urban and rural communities in sub-Saharan Africa, the Carribean region, and South America.1 Tunga penetrans infests a broad range of sylvatic, domestic, and pet animals, such as monkeys, cows, pigs, goats, cats, and dogs.2–7 In addition, at least in northeastern Brazil, Rattus rattus has been frequently found to be infested.3 Because of the zoonotic characteristics of this ectoparasitosis, it is difficult to establish the role various animal reservoirs have on human infestation. It is assumed that different animal species contribute to the spread of the parasite in a complex manner that depends on the environmental, social, and economic characteristics of a disease-endemic area. For example, in an urban squatter settlement in Brazil, dogs, cats, and R. rattus were identified as the most important reservoirs, with 67%, 50%, and 42% of the animal species, respectively, being infested.3
The older literature has many anecdotal reports suggesting that newcomers to a disease-endemic village got heavily infested, usually at night, when they stayed in shelters used by animals, abandoned huts, or houses not well maintained in which organic waste littered the soil.8,9 These shelters did not have solid floors, doors and windows, if any, were kept open so that domestic animals could freely move in and out. Roofs were not tight, which allowed rodents to enter at night. Obviously, these circumstances would facilitate the establishment of an intradomiciliary life cycle of T. penetrans, even in the absence of inhabitants. However, whether infestation actually occurs indoors has never been properly investigated. A recent study indicated that housing and the absence of a concrete floor are important risk factors for severe infestation and contributed to the suggestion that indoor transmission is important.10 As part of a comprehensive study on the epidemiology of tungiasis in northeastern Brazil, we attempted to address this issue by exposing laboratory-raised Wistar rats suitable for the on-host development of T. penetrans in different microenvironments.
The study was conducted in the fishing village of Balbino on the Atlantic Ocean (4°01'S, 38°13'W) in Ceará State in northeastern Brazil. The study area has been previously described.11 Briefly, the village is located on a dune and houses are situated on rather large compounds (average = 500 m2). Houses are constructed from brick, adobe, or palm stems covered with palm leaves. Floors are made from concrete or tiles, or consist of stamped clay or bare sand. Rattus rattus has never been observed in the village, but small sylvatic rodents are sometimes seen at night. Many families keep dogs and cats as pets. The soil is sandy. Tungiasis is hyperendemic in the area, with a prevalence of 51% in the dry season.11
In October 2002, 30 laboratory-raised Wistar rats (four weeks of age and weighing 180–200 grams) were put into six cages and exposed to T. penetrans in six different compounds. Compounds belonged to households where at least one member was affected by tungiasis at the time of investigation. Wistar rats have been shown to be appropriate animals for artificial infestation with T. penetrans (Witt L, unpublished data). The cages were placed on the ground in such a way that the animals were in direct contact with the soil. Cages were placed at different locations for a period of 14 days. Each of the locations represented a particular microenvironment (Table 1
). The soil was bare sand at all sites. Exposure in full sun was avoided because the temperature at the surface of the soil may reach more than 40°C, a temperature at which the animals would have suffered and possibly died of exsiccation. Animals received food and water ad libitum.
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Embedded sand fleas were exclusively observed in rats exposed in cages placed outside (Table 2). No penetration occurred in rats in cages placed in the living room and kitchen of two households. Eighty percent of the rats kept in an open kitchen stall and all rats kept in a cage placed at the far end of a compound became infested. A total of 83% of rats exposed under a mango tree showed embedded sand fleas (difference of proportions was not significant). The median number of lesions caused by flea infestation varied significantly between the six cages (P < 0.01 ). It increased from 0 (range = 0–1) per rat in a cage placed immediately near the wall of the house to 7 (range = 4–17) in animals exposed at the far end of a compound (Figure 1).
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Although we did not show that transmission occurred indoors, rats exposed on the ground of an open kitchen stall became heavily infested. In these types of kitchens, organic material litters the soil and domestic animals move in and out. This movement could shed eggs expelled from embedded sand fleas. Both characteristics would facilitate off-host development to occur. These types of constructions are similar to those described in previous reports on rapid human infestation, in which foreigners arrived in disease-endemic areas.8,9,12,13
The off-host development of T. penetrans starts when eggs are expelled from embedded fleas and fall to the ground. Three to four days after eggs have been shed, the first instar larva develops and starts to feed on organic material present in soil.14 In contrast to other flea species, T. penetrans has only two larval stages and one nymphal stage. Pupae develop into adults approximately 18 days after eggs have reached a suitable place for development.15 The physical and chemical characteristics of soil needed for successful completion of the off-host part of the life cycle of T. penetrans are not well known. However, circumstantial evidence indicates that dry soil containing organic material such as household detritus or decaying leaves is an excellent habitat for the parasite.1,16
A risk factor study performed in the village showed a fourfold increased risk for the presence of tungiasis in households when the house was constructed from crude adobe or palm stems and an eight-fold increase for houses with a floor consisting of sand.10 This also points to the importance of a particular micro-environment for the transmission of T. penetrans and could indicate indoor transmission. However, indoor transmission was not observed in this study, although the small number of experiments does not allow a definitive conclusion. If transmission mainly occurs outdoors, this has important implications for preventive measures. It would be appropriate to spray the ground with a contact insecticide where pets frequently rest, but it would not be reasonable to spray the floors of houses.
Received September 21, 2006. Accepted for publication October 25, 2006.
Acknowledgments: We thank Michi Feldmeier for secretarial assistance.
Financial support: The study was supported by a grant from Bayer Crop Science (Monheim, Germany).
* Address for correspondence: Hermann Feldmeier, Institute of Microbiology and Hygiene, Charité University Medicine, Campus Benjamin Franklin, Hindenburgdamm 27, D-12203 Berlin, Germany. E-mail: hermann.feldmeier{at}charite.de 
Authors’ addresses: Lars Witt, Stefan Schwalfenberg, and Hermann Feldmeier, Institute of Microbiology and Hygiene, Charité University Medicine, Campus Benjamin Franklin, Hindenburgdamm 27, D-12203 Berlin, Germany, Fax: 49-4181-36943, E-mails: wittlars{at}web.de, sschwalfenberg{at}web.de, and hermann.feldmeier{at}charite.de. Jörg Heukelbach, Department of Community Health, School of Medicine, Federal University of Ceara, Rua Professor Costa Mendes 1608, Fortaleza CE 60931-140, Brazil, Fax: 55-85-278-3093, E-mail: Heukelbach{at}web.de. Ronaldo A. Ribeiro, Department of Pharmacology and Physiology, School of Medicine, Federal University of Ceara, Av. Cel. Nunes de Mela 1315, Fortaleza CE 60430-270, Brazil, Fax: 55-85-3366-8333. Gundel Harms, Institute of Tropical Medicine, Charité University Medicine, Spandauer Damm 130, 14050 Berlin, Germany, Fax: 49-30-30102743, E-mail: gundel.harms{at}charite.de.
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