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Editorial: Cutaneous larva migrans and tungiasis: the challenge to control zoonotic ectoparasitoses associated with poverty

2002; Wiley; Volume: 7; Issue: 11 Linguagem: Inglês

10.1046/j.1365-3156.2002.00961.x

1365-3156

Jörg Heukelbach, Norbert Mencke, Hermann Feldmeier,

Cultural Competency in Health Care

The great majority of tropical diseases is – in one way or another – intricately linked to poverty. There is convincing evidence that, for example, intestinal helminthiases, systemic worm diseases such as schistosomiasis and lymphatic filariasis, but also protozoal and bacterial diseases (among others, malaria, amoebiasis, Chagas disease and tuberculosis) are disproportionally more common in poor populations and that the morbidity associated with these infections is particularly high in deprived communities (Bradley 1997; Guerrant & Blackwood 1999; Traub et al. 2002). The complex relationships between poverty and parasitic infections are well recognized, and initiatives addressing these issues have been in existence for a long time. The African Onchocerciasis Control Program, the Southern Cone Initiative against Chagas disease, the Intestinal Helminths Control Program and the Roll Back Malaria Program, to name just a few, are goal-oriented programmes conceived to relieve poverty-stricken populations from the burden of parasitic diseases (Kumate 1997; Albonico et al. 1999; Colley 2000). It therefore comes as a surprise that ectoparasitoses, a group of parasitic diseases which have afflicted poor populations since ancient times, are not even mentioned when important health threats and means for interventions are discussed (Visschedijk & Siméant 1998; Colley 2000). By consequence, the issue of ectoparasite control in deprived populations has rarely been addressed and was never dealt with comprehensively (Taplin et al. 1991; McCrindle et al. 1996; Carapetis et al. 1997; Figueroa et al. 1998). Of the six major parasitic skin diseases – human scabies, pediculosis, flea infestation, tungiasis, cutaneous larva migrans (CLM) and myiasis – only the first two are not zoonoses. Whereas for scabies and pediculosis, control measures only need to target the human host, the other ectoparasites require consideration of an animal reservoir. Obviously, the existence of an animal reservoir together with a complex life cycle make interventions more challenging. Cutaneous larva migrans (creeping eruption) is caused by penetration of hookworm larvae, usually from dogs or cats, into the skin of humans. Infection occurs after contact with soil contaminated by animal faeces. As man is not an appropriate host, larvae cannot reach their programmed destination and migrate in the epidermis for up to several weeks. Thus, creeping eruption is a self-limited disease. However, as almost invariably itching is severe, CLM disturbs the patient's sleep for a prolonged period. Secondary infection, particularly because of scratching, is common in poor settings (J. Heukelbach, unpublished observation). Cutaneous larva migrans is endemic in many poor communities in tropical and subtropical countries and sporadically occurs in temperate climates (Roest & Ratnavel 2001; Klose et al. 1996). In scientific literature CLM is usually referred to as an exotic disease of travellers returning from the tropics where tourists acquire the infection on beaches frequented by stray dogs (Jelinek et al. 1994; Blackwell & Vega-Lopez 2001). Outbreaks in groups of tourists with more than a hundred infected individuals have been reported (Tremblay et al. 2000). The only risk factor identified so far is walking barefoot (Tremblay et al. 2000). Surprisingly, even in textbooks the disease is not mentioned as a typical plague of deprived populations. Close human bonds with dogs and cats infected with Ancylostoma spp. explain the frequent occurrence of human disease in areas where these animals are not treated with anthelminthics. In endemic areas, dogs are heavily infected with hookworms, and prevalence rates of ancylostomiasis may range from 20% to almost 100% (Malgor et al. 1996). There are no reliable prevalence data of CLM at population level. In two community-based studies in an urban slum and a poor fishing community in North-east Brazil we found point prevalence rates between 1% and 3% with all age groups being similarly affected (T. Wilcke, unpublished observation). Tungiasis is caused by penetration of the female sand flea Tunga penetrans into the epidermis and its subsequent hypertrophy. Similar to CLM, tungiasis has received attention as an exotic infection in the returning traveller, and attempts to understand the biology of the parasite and the epidemiology of the disease are scant (Hicks 1930; Geigy & Herbig 1949; Matias 1988). Bacterial super-infection is very common, and severe tungiasis seems to be a risk factor for contracting tetanus in areas where immunization coverage is low (Obengui 1989; Feldmeier et al. 2002). Other sequels include loss of toenails, deformation and auto-amputation of digits (Heukelbach et al. 2001). Incidental observations indicate that infection occurs mainly in the shade, for example under trees or inside houses without paved floors, particularly in areas where pets prevail and where the soil is littered with rotting organic material (J. Heukelbach, unpublished observation, 2001). The parasite is endemic in many Latin American, Caribbean and sub-Saharan African Countries (Heukelbach et al. 2001). In poor communities in Brazil, Trinidad and Nigeria, point prevalence rates between 16% and 54% have been reported (Ade-Serrano & Ejezie 1981; Chadee 1998; Wilcke et al. 2002). In the urban environment, dogs and cats act as reservoirs for T. penetrans. In a survey in a slum in North-east Brazil, 67% of dogs and 50% of cats were found to be infected, many of the animals harbouring dozens of fleas (J. Heukelbach, unpublished observation). Rodents also seem to be an important reservoir. We found tungiasis in 59% of Rattus rattus captured in a poor neighbourhood (J. Heukelbach, unpublished observation). In the countryside, pigs and cattle are known reservoirs for T. penetrans (Vaz & Rocha 1946; Verhulst 1976). Interestingly, community health workers observed a significant reduction of attack rates in humans after the prohibition to let pigs freely roam in the community as well as after plague control measures, which had reduced the rat population (R.C. Sabóia-Moura, personal communication, 2001). However, no data are available indicating to what extent the various animal reservoirs contribute to high human attack rates. Clearly besides general measures such as environmental sanitation the control of CLM and tungiasis requires various additional approaches. As man is a dead end and larvae do not develop further in the human host, treatment of humans does not have any impact on the transmission of CLM. Hence treatment of the animal reservoir is crucial for CLM control. Clear recommendations have been published in the US by the Centers for Disease Control and Prevention to achieve the so-called ‘strategic deworming’ (CDC 1995). They include a series of anthelmintic treatments depending on the endemic situation. Studies have shown that co-operation between veterinary practitioners and physicians, especially paediatricians, is important in order to significantly lower the worm load in the pet population (Gauthier & Richardson 2002). However, the situation is different in the developing world where innumerable stray dogs roam the settlements, where pet owners are not aware of the importance of treating their animals, public veterinary health is deficient and financial constraints prohibit control measures. As a result, in poor communities health education enforcing the use of appropriate footwear and instructing pet-owners how to treat their animals with anthelminthics seem to be the best option for the prevention of CLM. As data on the importance of the various animal reservoirs on human attack rates are missing and no efficacious chemotherapy is currently available to kill embedded fleas, the control of tungiasis is even more difficult to achieve. Eggs, larvae and pupae may persist in the environment for weeks – if not months – and the reduction of an animal reservoir by treating animals with an antiectoparasitic compound yet to be identified presumably would not avoid rapid re-infection of man. Modern approaches of flea control combine the application of on-animal-products with other insecticides targeted at larval stages present in the environment. Recently introduced veterinary insecticides such as imidacloprid, fipronil or insect growth regulators such as pyriproxifen and methoprene work well against various species of pet fleas and should be tested for their efficacy against T. penetrans, as should be organophosphates and pyrethroids. As the flea seems to prefer sandy soil and shade for breeding, the floors of houses should be cemented and streets paved. Improved sanitation and regular waste collection will probably also contribute to reduce incidence and morbidity. However, these control measures are clearly costly and not feasible in many deprived communities. The impact of early diagnosis and rapid elimination of embedded fleas is demonstrated by an anecdotal observation (Jolly 1926). Soldiers in a military camp in East Africa had been so severely affected by T. penetrans that half of them could not walk anymore. Classical means of prophylaxis such as wearing boots during the whole day and spraying the whole area with a kerosene emulsion reduced the parasite burden and morbidity only insignificantly. Then, the soldiers were encouraged to walk barefoot, serving as living traps. Their feet were inspected every day for the presence of embedded fleas, which were then immediately extracted with a sterile needle. After one month, the number of fleas extracted daily per 100 soldiers had been reduced from 315 to five. Health education must focus on primary (using closed shoes wherever the environment is not paved) and secondary prevention, i.e. educating people to inspect their feet daily and take out embedded fleas with a sterile instrument. This, in turn, requires substantial impact from the health care system; as with other parasitic diseases, health education is a difficult task. In Brazil, for example, the issue is even more complicated. People consider tungiasis a nuisance rather than a disease and therefore tend to neglect this ectoparasitosis (J. Heukelbach, unpublished observation). In Brazil many poor communities are covered by the so-called Family Health Program (FHP). The FHP provides primary health care and encourages community participation, health education and teamwork between health professionals and community health workers. Since the introduction of the FHP, the health situation of poor communities especially in northeast Brazil has improved significantly. It seems that such a FHP has the appropriate infrastructure to respond to morbidity problems caused by ectoparasites in communities with poor resources. Obviously reliable and rapid measures need to be taken to determine the burden of CLM and tungiasis before and after intervention. Sentinel animals seem to be useful indicators of local transmission dynamics of tungiasis. When laboratory-raised Wistar rats were exposed in cages placed in sandy soil, attack rates correlated with prevalence rates in neighbouring families (J. Heukelbach, unpublished observation). Rapid assessment of CLM essentially depends on the disease perception and healthcare seeking behaviour of the affected population. In North-east Brazil, individuals with CLM frequently present to local primary health care centres. Thus, screening patients attending the health posts of the endemic area will give a reliable estimate of the prevalence of this ectoparasitosis in the community (Heukelbach, unpublished observation). In conclusion, only an integrated approach combining the control of the animal reservoirs, environmental control and health education will be successful. As CLM and tungiasis are zoonotic diseases embedded in the socio-cultural context of poverty, it is essential that intervention measures are designed by an interdisciplinary team of public health professionals, medical anthropologists, veterinarians and entomologists and that they are implemented in co-operation with the community. We also need to investigate the potential of modern insecticides to combat T. penetrans on the host and in the environment, and to increase our knowledge on the biology and epidemiology of both ectoparasites. This work was supported by the Ärztekomittee für die Dritte Welt, Frankfurt (Germany), World Health Organization grant CPE/PVC B′′/181/195, Geneva (Switzerland), Laboratórios Sintofarma S.A., São Paulo (Brazil) and Merck do Brazil, Rio de Janeiro (Brazil).