Parasitol Res (2005) 97:S113–S120 DOI 10.1007/s00436-005-1454-z
Field trial of the efficacy of a combination of imidacloprid and permethrin against Tunga penetrans (sand flea, jigger flea) in dogs in Brazil S. Klimpel1, H. Mehlhorn1 (✉), J. Heukelbach2, H. Feldmeier3, N. Mencke4 1Institute of Zoomorphology, Cell Biology and Parasitology, Heinrich-Heine-University, 40225 Düsseldorf, Germany 2Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil 3Department of Medical Microbiology and Immunology of Infection, Institute for Infection Medicine, Charité, Berlin, Germany 4Bayer HealthCare AG, Animal Health Division, Leverkusen, Germany
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Abstract In a field trial in Brazil 17 dogs penetrated by females of the jigger flea, Tunga penetrans, were topically treated with treated with a combination of 10% imidacloprid and 50% permethrin (Advantix®), while 17 dogs remained untreated. The follow-up controls on days 7, 14, 21 and 28 post-treatment clearly showed that, beginning from day 7, the flea load in treated dogs decreased, so that most of the dogs became free of tungiasis lesions, while in the untreated group the flea load remained high. Since the dogs distribute the flea eggs throughout the village, leading to a high incidence of tungiasis in humans, treatment of dogs probably also decreases the number of cases of tungiasis in the latter.
Introduction Tungiasis is a disease caused by the penetration of the female jigger flea or sand flea, Tunga penetrans, into the skin of its host, which includes humans, dogs, cats, pigs and cattle (Eisele et al.2003; Muehlen et al.2003; Heukelbach et al.2004; Trentini et al.2001;Vobis et al.2005).The flea undergoes a peculiar hypertrophy, which begins during penetration of the skin; after some days the abdominal segments have enlarged up to the size of a pea. Countless eggs are expelled during a period of about 3 weeks (Eisele et al. 2003). After all the eggs have been expelled, the involution of the lesion begins. Four to six weeks after penetration, the parasite dies and is sloughed from the epidermis by tissue repair mechanisms (Feldmeier et al. 2004).
Tungiasis is a zoonosis that originally occurred exclusively in South America and the Caribbean Islands. The fleas spread from these areas to Africa in ballast sand in ships (Henning 1904). Within a few decades T. penetrans had spread from Angola along trading routes and with advancing troops throughout entire sub-Saharan Africa, including areas with tropical rainforest (Heukelbach et al. 2001, 2002, 2004). At the end of the nineteenth century the sand flea reached East Africa and Madagascar. Recently, tungiasis has become endemic in many countries of the American continent and ranges from Mexico to northern Argentina (Mehlhorn 2001). Within the endemic areas the parasitosis has a patchy distribution; it occurs in under-developed communities in the hinterland, in solitary fishing villages along the Atlantic coast and in the slums (favelas) of urban areas. Tungiasis is especially associated with the presence of dry sandy soils. Similar to other parasitic skin diseases, such as scabies, the occurrence of severe tungiasis is linked to poverty. In Brazil, prevalence rates reach up to 40% in the favelas, as well as in the underdeveloped hinterland. Since T. penetrans is unable to jump very high, generally lesions are confined to the feet. Infection with T. penetrans is intensely irritating to the host and the disease causes considerable morbidity, with sequelae such as secondary infections, lymphadenopathy, deformation of fingers and feet and loss of toenails (Feldmeier et al. 2004; Heukelbach et al. 2001, 2002, 2004). In endemic areas, domestic animals – especially dogs and cats – are frequently infested and harbour T. peneS113
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trans at prevalence rates comparable to those in the human population (Heukelbach et al. 2004). Since the dogs and cats as well as rats roam throughout the living rooms of humans – where the dwellings are in a locality with sandy soils – the eggs dropping from female fleas which have penetrated the animals are a permanent source of flea development and the subsequent infection of humans. Therefore, as a first step in the successful control of tungiasis in deprived communities of North-east Brazil, and towards the development of effective measures for its prevention and control, domestic dogs were treated with a combination of 10% (w/v) imidacloprid and 50% (w/v) permethrin (Advantix).
Materials and methods Area under investigation The present study was performed in the fishing village of Balbino, approximately 65 km south of Fortaleza, the capital of Ceará State (north-east Brazil). Balbino is situated on sand dunes near the coast of the Atlantic, and the village inhabitants generally depend on fishing for their livelihood. The community currently comprises 141 families with a total of 605 inhabitants. The population is regarded as poor, according to WHO standards, but does not suffer from starvation. The village streets are not paved and many houses are built on sandy soil. About 75% of the households have electricity and 87% possess a latrine. Slightly more than 84% of the families have a domestic dog. On average there are 1.5 dogs per family.
each household were thoroughly examined for the presence of T. penetrans (stage 3 lesion). In cases of the temporary absence of a dog, the family was visited twice. Photographs were taken of all dogs in order to be able to identify them clearly. All diagnoses were made clinically. The following finding was considered to be diagnostic for tungiasis in dogs: circular lesions presenting as a white patch, diameter 4–10 mm, with a central black dot showing posterior segments of a mature female T. penetrans (mature stage, stage 3). Tungiasis was seen to occur on virtually every part of the dog. For this reason the following parts of each dog were examined: feet, abdomen and head. However, most of the fleas which had penetrated the dogs occurred on the legs. A total of 15 jigger females were excised from dog pads and examined for determination of the Tunga species using the exterior diagnostic taxonomic characters. All specimens were confirmed as T. penetrans. Altogether 34 dogs penetrated by T. penetrans were chosen, the four legs of individual dogs had up to 43 fleas which had penetrated the skin. While 17 randomly selected dogs were treated with Advantix according to label instructions (single application), 17 other dogs remained untreated as a control group. Fifteen dogs in both groups finished the study; two dogs in each group were euthanized for unknown, non-study-related reasons and thus did not appear for re-examination.
Ethical considerations Permissions to perform the studies in the fishing village of Balbinos (Fortaleza) were obtained from the Community Associations of Balbino and from Cascavel Municipality.
Study design The investigation was based on home visits to the population. All households of the investigated area were visited by two investigators responsible for the examinations of dogs and additionally of humans. Surveys were made during April and May 2005, when the attack rates of T. penetrans are high in the human population. After explaining the objectives of the study and obtaining oral consent from the head of the family, the dogs of S114
Results In the fishing village of Balbino, the prevalence of tungiasis was high in dogs and in children. In both hosts the tungiasis lesions were mainly found along the extremities and only rarely in other places (Figs. 1, 2, 3), e.g. in the nipples of female dogs.
At least two stage-3 females which had penetrated the skin where found in the legs of the dogs. However, often many more lesions occurred (Table 1). Up to 43 fleas were found on individual dogs; as a consequence these dogs had difficulties in walking (Fig. 4). The 17 dogs selected randomly for the control had a total of 197 fleas prior to treatment, while a total of 132 fleas were visible on the 17 dogs of the Advantix-treated group (Table 1, Fig. 5).
Fig. 1. Tungiasis lesions in the foot of a child of dog owners in Balbino
Fig. 2. Tungiasis lesions in a dog’s foot
On day 7 after treatment all dogs were thoroughly inspected for the number of viable tungiasis lesions. One dog of the untreated group was euthanized by its owner, and four did not appear for the inspection (two of the treated group and two of the untreated group). The 15 dogs of the treated group investigated showed a total of 47 fleas,while the 14 dogs of the untreated group had 168 fleas (Fig. 5). While in the untreated group all dogs had the same high number of tungiasis lesions, six dogs of the treated group already showed only one or even an absence of tungiasis lesions. On day 14 after treatment two further dogs (one of each group) had been euthanized by their owners. In addition one dog of each group did not appear at the examination point. The 15 dogs of the treated group showed a total of only three tungiasis lesions, while in the 14 untreated dogs 132 fleas which had penetrated the skin, were still noted (Fig. 5). Thus, except for three dogs with only one tungiasis lesion, all the other dogs were free of Tunga, while in the untreated group the individual flea load remained high (up to 20 per dog). On day 21 after treatment another dog was euthanized and only one dog did not appear for the examination (Table 1). The treated 14 dogs showed a total of 12 fleas. Thirteen dogs were free of tungiasis lesions or had only one at most, while the 14 dogs of the control group had 113 tungiasis lesions and no dog was free of fleas (Table 1, Fig. 5).
Fig. 3. Tungiasis lesion in a female dog’s nipple
On day 28 after treatment only one dog did not appear for examination. The 14 control dogs showed, in total, penetration by a huge number of fleas, 180, while in the 15 dogs of the treated group a total of 38 fleas was found (Table 1, Fig. 5). Eight dogs still had no or one tungiasis lesion at most.
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the product which are stored in the fine sebaceous surface layer of the host’s body. Thus the results of the present investigation were not expected at the beginning of the experiments, since the Tunga fleas penetrate the feet of dogs (often between the toes or on the surface of the ball), where in general no or only a little fatty sebaceous material is retained that could store the insecticide.
Fig. 4. Cachectic dog with multiple infections including Tunga penetrans
The observed effect of the imidacloprid/permethrin combination in protecting dogs from the penetration of sand fleas is probably explained by the observation of Nagy et al. (2005), that both male and female fleas roam in the hair of the dogs and start to suck blood at smooth places on the skin. When imidacloprid and permethrin are present, females (Fig. 6) are killed well before they approach their preferred sites on the host’s feet. The males (Fig. 6) probably are also killed quickly and thus are unable to copulate with females which have already penetrated the dog. This significantly reduces the likelihood of egg production. The reduction in the flea load only progressed slowly because the dogs were naturally infected at the beginning of the experiments; a total 47 fleas were found in the treated group on day 7. The efficacy of the imidacloprid/permethrin combination against fleas reported earlier corresponds well with the findings reported in this study on T. penetrans.
Fig. 5. Diagram of flea infestation (counts at different times after the treatment on day 0)
Discussion Advantix consists of two insecticides – imidacloprid and permethrin – and is known for its significant repellent and parasiticidal effects against fleas, ticks and sand flies (Mehlhorn et al. 2001, 2003; Krämer and Mencke 2001; Mencke et al. 2003; Hansen and Londershausen 2001).
Dogs, which are present in every family of the village investigated, are thought to be definitely the main vectors/distributors of sand fleas that penetrate humans there. From our molecular biological studies we know that the same species, T. penetrans (or even a subspecies?), can occur in dogs and humans (Vobis et al. 2005). Since the eggs laid by the female fleas drop constantly from the infected legs of dogs, the latter distribute eggs throughout the dwelling of their owners and throughout the whole village, when they are moving around. Since the larvae develop quickly into adult fleas, the flea load of children running around with bare feet or sandals is enormous.
This activity is explained by the fact that fleas, ticks and sand flies live on the skin or in the hair of their hosts and thus come into contact with the two components of
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Fig. 6. Scanning electron micrographs of a male and a female Tunga penetrans flea
Conclusion The results reported here suggest that constant treatment of the dogs with 10% (w/v) imidacloprid/50% (w/v) permethrin protects the dogs from sand flea penetration. Protection of dogs from T. penetrans would most probably significantly reduce the infection rate in humans, especially in children, that live in close contact with their dogs. Therefore proper use of effective veterinary medical remedies may have a significant impact on human health in these communities and should thus be considered in any health regime, e.g. for the prevention of the reported infections due to T. penetrans.
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