Transactions of the Royal Society of Tropical Medicine and Hygiene (2006) 100, 970—974
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Tungiasis in rural Haiti: a community-based response J. Keith Joseph a,∗, Junior Bazile b, Justin Mutter c, Sonya Shin a, Andrew Ruddle c, Louise Ivers a, Evan Lyon a, Paul Farmer a a Division of Social Medicine and Health Inequalities, Brigham and Women’s Hospital, 1620 Tremont Street, 3rd Floor, Boston, MA 02120, USA b Zanmi Lasante, Port au Prince, Haiti c Partners in Health, 641 Huntington Avenue, Boston, MA 02115, USA
Received 8 October 2005; received in revised form 26 November 2005; accepted 28 November 2005 Available online 6 March 2006
KEYWORDS Tungiasis; Tunga penetrans; Community health worker; Haiti
Summary Tungiasis is a disease endemic to poor communities in Latin America, the Caribbean and Africa. It is caused by the female flea, Tunga penetrans, which burrows into the skin of its host to feed while producing and extruding eggs. Consequent lesions may be painful and even crippling with damage ranging from mild erythema and swelling to necrosis. Superinfection of lesions can be serious and may result in auto-amputation or death from tetanus. We describe an outbreak of tungiasis in rural Haiti and a community-based intervention used to address it. Of 177 patients assessed, 132 (47 female, 85 male, 23 children) had tungiasis lesions. Fortyfour patients had clinical signs of superinfection; 15 had ectopic lesions. Community health workers cleaned and disinfected patients’ feet and any parts of the body with ectopic lesions, and then extracted fleas from existing lesions. Patients with superinfections were treated with appropriate antibiotics. Over 1000 pairs of shoes were distributed in the villages. Over 400 adults were given tetanus vaccinations during follow-up visits. Patients who had been treated reported feeling better and those who had received shoes indicated they had not developed new lesions. All superinfections were resolved. We concluded that community-based care can treat tungiasis effectively. © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
1. Introduction Tungiasis is an ectoparasitic disease caused by the sand flea, Tunga penetrans, which is endemic to Latin America, the
∗
Corresponding author. Present address: Division of Infectious Diseases, Columbia Presbyterian Medical Center, 622 West 168th Street, PH-8, New York, NY 10032, USA. Tel.: +1 212 305 7185; fax: +1 212 305 7290. E-mail address:
[email protected] (J.K. Joseph).
Caribbean and sub-Saharan Africa. This flea is known to infect humans, and several domestic and sylvatic animals. First recorded in 1525 by Gonzalez Fernandez de Oviedo y Valdes among Spanish sailors left on Hispaniola after Columbus’s first journey, there have been many additional reports of tungiasis in disease-prone communities of South America and the Caribbean over the centuries (Guerra, 1968; Hoeppli, 1963). The spread of tungiasis from the Americas to Africa is attributed to the Thomas Mitchell, a ship which sailed from Brazil to Angola in 1872; it is thought to have carried the flea among its sailors and in the sand it carried
0035-9203/$ — see front matter © 2005 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2005.11.006
Tungiasis in rural Haiti: a community-based response for ballast (Gordon, 1941; Hoeppli, 1963). The disease then spread along the west coast of Africa, into the interior and as far as the eastern coast of the continent. Tungiasis continues to afflict poverty-stricken communities in countries where it is endemic. The free-living flea’s average length is approximately 1 mm. It is a poor jumper, capable of reaching heights of only about 20 cm. The life cycle of the male flea consists of freeliving blood sucking and mating with females. The female starts as a free-living blood feeder and then penetrates the skin of her host, leaving the hindquarters exposed for respiration, defecation and extrusion of eggs. The characteristic black dot on the surface of lesions is the hindquarters of the female. After penetration the flea undergoes hypertrophy, increasing its size by approximately 2000—3000 times over about a 10-day period. At this point, the typical skin lesion is a 0.5—1.0 cm white spot with a black dot in the middle. The female flea can harbor up to 200 eggs at any given time. Released eggs hatch to form T. penetrans larvae after approximately 3—4 days. The larvae prefer shady, dry areas and feed on organic material. The larvae next pass through a pupal stage and then into fully developed sand fleas, which re-infect the host to complete the cycle (Eisele et al., 2003; Heukelbach et al., 2001). Skin lesions caused by T. penetrans can be debilitating. The female’s protruding hindquarters serve as an entry point for pathogenic bacteria, leading to superinfection (Feldmeier et al., 2002; Heukelbach et al., 2001). Most infections in humans occur on the feet, particularly in the periungual skin of the toes, for which T. penetrans appears to have a preference. Ectopic infections at other sites, most commonly on the hands, have been reported (Heukelbach et al., 2002; Muehlen et al., 2003). Most reports of tungiasis describe cases of travelers from developed countries who return from endemic areas with mild infestation. While considered a nuisance to travelers in developed countries, its prevalence in some of the poorest regions in the developing world — both urban and rural — often goes unconsidered. In endemic communities, superinfection can result in severe and disabling cases. Low socioeconomic conditions are primary catalysts to infestation: poor sanitation, unpaved public thoroughfares, housing with dirt floors, and walking or working barefoot due to lack of or inadequate footwear. Children in the 5—10 years age group are among those most commonly infested (Chadee, 1994; Feldmeier et al., 2002; Muehlen et al., 2003). Bacterial superinfection can lead to tissue necrosis, auto-amputation of digits, sepsis and, in unvaccinated persons, tetanus that can result in death (Feldmeier et al., 2002, 2003; Litvoc et al., 1991; Tonge, 1989).
2. Tungiasis and intervention in rural Haiti Haiti is the poorest nation in the Western Hemisphere and one of the poorest on earth. The annual per capita income in Haiti is approximately US$1107. There are 1.2 doctors and 1.3 nurses for every 10 000 inhabitants. Forty percent of the population remains without access to any form of primary health care. Approximately half the population is illiterate. General life expectancy is 51 and dropping (CIA, 2004). Demographic figures are much worse in Haiti’s
971 mountainous Central Plateau, the poorest region in the country. It is in this setting that we report on endemic T. penetrans and an initial public health response to it. The intervention occurred in the rural commune of Boucan-Carr´ e, a mountainous region (approximate surface area, 399 km2 ) of the Central Plateau (average altitude 396 m). The commune’s 50 000 inhabitants are currently served by a new hospital built by the non-governmental organization Partners in Health and managed in partnership with the Haitian Ministry of Health. Partners in Health is a non-profit organization based in Boston, Massachusetts, USA, which, in collaboration with its Haitian sister organization, Zanmi Lasante, has been providing comprehensive healthcare throughout Haiti’s Central Plateau since 1985. Given the low ratio of doctors and nurses to population in rural Haiti, community health workers have always been an important component of the health care services provided by Partners in Health. Community health workers are trained in the administration of vaccines, recognition of signs and symptoms of specific diseases, and the provision of directly observed therapy (DOT) for tuberculosis. Since 1998, they have also been trained in providing DOT for antiretroviral therapy to treat AIDS. In 2002, Haiti received US$66.9 million from the Global Fund against AIDS and tuberculosis. The construction of the hospital in Boucan-Carr´ e was part of the project to expand Global Fund AIDS and tuberculosis treatment. Although concerns have been raised that treating AIDS would drain already limited resources from other programs, our experience has been that expansion of AIDS treatment has led to improvements in primary health care in general (Walton et al., 2004). The intervention made to treat and prevent complications from the tungiasis epidemic is an example of how the communitybased AIDS treatment expansion program has improved care for other diseases. According to local accounts, tungiasis, known as chik in Haitian Creole, has persisted for several decades predominantly among four villages in Boucan-Carr´ e’s northern mountains, the Petites Montagnes (highest elevation 1323 m). The four villages, Bouly, Decid´ e, Bois Rouge and La Borde, are clustered on the western limit of the commune of BoucanCarr´ e, but each village is separated from the others by mountains. There is a common road to Bouly one must pass along to arrive at Decid´ e and La Borde. Bois Rouge lies on a separate road to the northeast of the other three villages. Most residents of these areas live between elevations of approximately 427 m and 640 m. Government census data and hospital census data from the region are limited and inexact, and boundaries of the villages are often disputed. There are approximately 600 families living among the four villages, with a combined population estimated at 3600 people. Bouly and Bois Rouge each have about 1200 residents. Decid´ e has an estimated 700 residents and La Borde between 500 and 600. The population of each village is spread over a wide territory and up the sides of the mountains. The outbreak was first assessed by Zanmi Lasante’s clinical staff in March 2004, during the end of Haitian dry season. The community health workers working in the region brought the epidemic to the attention of the clinic staff. The clinic staff’s awareness of the outbreak was delayed in part due to the relative isolation of the Petites Montagnes. Affected
972 Table 1
J.K. Joseph et al. Patient distribution by age and sex Age (years) <5
Male Female Total
5—10
11—15
16—30
31—50
>50
Not given
Total
8 4
6 5
0 0
18 10
36 17
6 9
11 2
85 47
12
11
0
28
53
15
13
132
regions lie on the frontiers of the health district, with timemeasured distances from the hospital ranging from 6 to 20 h on foot. There are no roads traversing the Petites Montagnes, and some paths are even impassable to pack animals. Travel to each of the villages requires traversing at least four rivers, several of which become impassable after rainfall. Regional poverty is pervasive; most inhabitants of afflicted villages cannot afford even basic footwear. Vaccine coverage for children and pregnant women has been complete in three of the villages and partial in a fourth. None of the villages had campaigns to vaccinate adults for tetanus prior to this intervention. The first step in the intervention consisted of organized mobile clinics that traveled to afflicted villages. Several weeks prior to arrival of the mobile clinics, community health workers began informing residents of the villages about the dates and purpose of the mobile clinics. Supplies were carried on pack animals, and teams of one or two doctors, a nurse, volunteers and community health workers set up treatment stations. One full day was spent working in each of the region’s four main villages. Patients were self-referred, after having been informed in advance of the mobile clinics. Tungiasis lesions were diagnosed based on clinical aspects of the Fortaleza Criteria, described elsewhere (Eisele et al., 2003). Patients’ feet, as well as any parts of the body with ectopic lesions, were cleaned and disinfected. Tunga penetrans fleas, often in hypertrophied state, were then extracted from existing lesions, using number 11 and 15 scalpel blades. Most of the community health workers were already experienced in both identifying and extracting embedded fleas. The familiarity of the local populations with extraction has been described in early reports (Gordon, 1941). Community health workers were trained in sterile technique during this intervention. All patients treated by community health workers were also examined by a doctor before and after lesion removal. Necrotic tissue was debrided and all patients with evidence of superinfection were treated with either trimethoprim/sulfamethoxazole and metronidazole, amoxicillin and metronidazole, or amoxicillin/clavulanate. Over 1000 pairs of shoes were distributed in the villages. Patients with severe infestations or superinfection were prioritized to receive shoes, but additional shoes were distributed in an effort to help limit further infestation. Tetanus vaccination was provided to over 400 adults in a series of follow-up visits by the community health workers. No evaluation was performed on pigs, dogs or horses because of time limitations. In all, 177 total patients were assessed and 132 of these patients determined to have tungiasis lesions requiring treatment. Of these 47 were female and 85 were male, including 23 children below the age of 10. Ages were not
recorded for several patients who could not remember or even approximate their birth dates. Age statistics for the remaining 119 patients showed that the highest prevalence was in older adults (Table 1). Thirteen patients presented with more than 10 lesions, including 7 who presented with more than 30 lesions. Fifteen had ectopic localization at sites other than the feet. Fourteen of the patients with ectopic lesions had lesions on the hands, and one, a 42year-old man, had a single lesion on the back of his thigh. Forty-four were treated for signs or symptoms of superinfection with one of the above regimens (Table 2). Four deaths from tungiasis-induced superinfections, all in adults over 30 years of age, were reported by community health workers during the period between May and July of 2004. None of these patients were seen by a physician. All reportedly had heavy infestations on their feet that caused difficulty walking. The descriptions given by the community health workers of three of the patients described rigid jaws and convulsions suggestive of tetanus. The other had high fevers and became unresponsive and died after three days. All patients with superinfection were targeted on followup visits by the nurse, health workers and volunteers, conducted between three and five weeks after the intervention. All of these patients resolved their superinfections and had no new lesions. Informal reports by patients who had been given shoes indicated that they had not developed new lesions. Patients who were treated reported feeling better after the intervention, but there were many complaints by the residents who did not receive shoes that they were not protected from infestation. Additional complaints and concerns were raised by those adults who were not vaccinated for tetanus and by community health workers that the incomplete vaccination coverage would lead to further complications. Each community requested more frequent and extensive interventions. Poor housing, vaccinations and footwear were among specific concerns that were
Table 2 Age and sex characteristics of patients with ectopic lesions Female
Male
Total
<5 years 5—10 years 11—15 years 16—30 years 31—50 years >50 years
2 1 0 1 0 1
5 2 0 0 2 1
7 3 0 1 2 2
Total
5
10
15
Tungiasis in rural Haiti: a community-based response raised. In each village these issues were raised in the context of requesting improvements in the overall availability and quality of health care and public health services.
3. Discussion Tunga penetrans is a disease that remains endemic to poor regions of nations situated in tropical climates. This is the first report of tungiasis in Haiti we are aware of since the first account from the island of Hispaniola by Gonzalez Fernandez de Oviedo y Valdes. Since this intervention, we have received several additional reports of tungiasis outbreaks from other regions of the country. The lack of essential public infrastructure, accessible basic health services, and generalized poverty contribute to the persistence of tungiasis in this region and present obstacles to its control and eradication. More community health workers have been trained in the sterile removal of the parasites, recognizing and treating superinfections with pre-packaged medicines, and tetanus vaccinations. Many of the interventions needed to successfully prevent and eradicate tungiasis are infrastructural and socio-economic in nature and lie beyond the scope of commonly available public health interventions in Haiti. This is also true of other diseases (e.g. correlations between HIV risk and basic education, TB and housing and food supplies, typhoid and other diarrheal illnesses and access to potable water, etc). The material and human resources put in place through the HIV and TB treatment expansion project provided an infrastructure to allow a substantial, communitybased intervention that provides care to the far reaches of the region. Using community health workers to fill the human resource gap in health care in the region has created a system that is successfully treating AIDS and tuberculosis, and that has demonstrated potential to respond to other health care needs effectively and comprehensively. In the case of tungiasis this will also require dedicating resources to housing, education, and evaluation and control of domesticated animal sources. There are many limitations to this intervention, most of which are consequences of the extreme poverty of the region. Firstly, essentially all of the houses have dirt floors. Housing renovation is available through the social assistance program, but is focused on patients with HIV and TB and has never been directed to the prevention of tungiasis. The patients in this series were predominantly older and male, which differs from most other reports (Chadee, 1994; Feldmeier et al., 2002; Muehlen et al., 2003). Self selection of patients in this report might account for this difference. Although patients appreciate and use the shoes given to them, they often will remove them inside their houses. People also routinely remove shoes to walk through mud and when crossing rivers, and often cross considerable stretches of dry land without replacing the shoes because of the inconvenience of constantly removing and replacing their shoes. This additional exposure of their feet to the ground can be large. Tetanus vaccine was given to only 400 people. Pregnant women and children have been receiving vaccine in this region since 2003, but this leaves a large number of unvaccinated adults. Some of the people own pigs, horses and dogs, and rats are ubiquitous; these animals provides a substantial potential reservoir for tungiasis. We were not able to
973 examine any possible animal reservoirs because of lack of time. Effective intervention will require all these issues to be addressed. This initial intervention will be used as a platform to perform both more comprehensive interventions in the future, and more thorough and detailed analysis of tungiasis and the results of interventions in the region. Using volunteers and community health workers, we should be able to make more comprehensive assessments of the prevalence of tungiasis in the region and pay attention to specific details of each patient. Some important considerations for future assessments include housing, detailing numbers and types of domestic animal reservoirs, the precise elevation at which families live and numbers of persons infested within households.
4. Conclusion Communities suffering from endemic tungiasis are inevitably severely economically depressed. Although the intervention described in this paper treated over 130 patients in remote areas, its effects will be temporary unless these efforts are continued and expanded. This initial assessment provided an overview of the problem, but more detailed assessment is needed to allow for better planning of interventions and measuring their effects. Vast infusions of material and human resources are needed if there is to be any hope of reducing and eventually eradicating tungiasis in this region. However, community-based care using community health workers can fill many of the short-term resource gaps and provide effective, primary health care services to treat cases of tungiasis using the model that has been successfully used to treat HIV and TB. Conflicts of interest statement The authors have no conflicts of interest regarding the work presented in this paper.
Acknowledgements Funding for this project was provided by The Division of Social Medicine and Health Inequalities, Brigham and Women’s Hospital, 1620 Tremont Street, 3rd Floor, Boston, MA 02120 and Partners in Health, 641 Huntington Avenue, Boston, MA 02115, USA.
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