Towards understanding the presence/absence of Human African Trypanosomosis in a focus of Côte d'Ivoire: a spatial analysis of the pathogenic system
© Courtin et al; licensee BioMed Central Ltd. 2005
Received: 25 August 2005
Accepted: 03 November 2005
Published: 03 November 2005
This study aimed at identifying factors influencing the development of Human African Trypanosomosis (HAT, or sleeping sickness) in the focus of Bonon, located in the mesophile forest of Côte d'Ivoire. A previous study mapping the main daytime activity sites of 96 patients revealed an important disparity between the area south of the town- where all the patients lived- and the area north of the town, apparently free of disease. In order to explain this disparity, we carried out a spatial analysis of the key components of the pathogenic system, i.e. the human host, the tsetse vector and the trypanosomes in their environment using a geographic information system (GIS).
This approach at the scale of a HAT focus enabled us to identify spatial patterns which linked to the transmission and the dissemination of this disease. The history of human settlement (with the rural northern area exploited much earlier than the southern one) appears to be a major factor which determines the land use pattern, which itself may account for differences found in vector densities (tsetse were found six times more abundant in the southern rural area than in the northern). Vector density, according to the human and environmental context in which it is found (here an intense mobility between the town of Bonon and the rural areas), may explain the observed spatial differences in HAT prevalence.
This work demonstrates the role of GIS analyses of key components of the pathogenic system in providing a better understanding of transmission and dissemination of HAT. Moreover, following the identification of the most active transmission areas, and of an area unfavourable to HAT transmission, this study more precisely delineates the boundaries of the Bonon focus. As a follow-up, targeted tsetse control activities starting north of Bonon (with few chances of reinvasion due to very low densities) going south, and additional medical surveys in the south will be proposed to the Ivoirian HAT control program to enhance the control of the disease in this focus. This work also shows the evolution of HAT regarding time and environment, and the methodology used may be able to predict possible sleeping sickness development/extinction in areas with similar history and space organization.
Human African Trypanosomosis (HAT) or sleeping sickness, is a vector-borne parasitic disease of Sub-Saharan Africa. The parasite (Trypanosoma brucei gambiense in West and Central Africa) is transmitted to humans by the bite of a dipteran insect, the tsetse fly (Glossina sp.). The disease, though almost eradicated in the early 60's, has once again become a major public health problem. Currently, about 60 million people are at risk of infection and around 300,000 are estimated to have the disease . Two principal parameters are usually put forward to explain this resurgence. First, the routine measures that were implemented to control the disease have gradually disappeared . Secondly, changes in the environment, through their effect on the relationships between host, vector and parasite, may also account for a significant part of the disease's re-emergence . In the forest area of Côte d'Ivoire, sleeping sickness has usually been associated with coffee and cocoa plantations . The establishment of these cash crop plantations, combined with massive immigration of agricultural labour, has altered the original habitat and caused the disappearance of the mainly zoophilic forest tsetse fly species, which have been replaced by vectors with a more opportunistic feeding pattern such as the main vector of sleeping sickness G. palpalis, that are able to adapt to peri-urban or urban areas [5–8]. The rise in numbers of agricultural workers also led to increased vector-host contact . The establishment of new villages (defined as inhabited by several families with a chief) and more especially new encampments (defined as inhabited by one family or by agricultural labourers, in coffee/cocoa plantations) also increased levels of movement along the new communication routes, further increasing human-vector contact [10–12]. Though such change is now widely accepted as a major cause of the development of sleeping sickness in the forest area of West Africa, it has yet to be discovered why the disease is present in some places but not in others, where demographic, behavioural and environmental conditions appear to be similar.
History of settlement
In this study, we have used information about parasitological, entomological, human and environmental factors, to describe and explain the substantial spatial disparity of HAT between the southern and the northern sectors of the Bonon focus. The results help explain the spatial evolution of HAT prevalence in the Bonon focus since the 1950s. The entomological study undertaken here has shown that in the southern rural area, the density of tsetse flies (Glossina palpalis palpalis) is much higher than in the northern rural area. The places of transmission are apparently located in the southern rural area, mainly in the south-eastern area, frequented by many rural and urban patients, and where numerous tsetse flies (among which 2.67% are infected by T. brucei) were caught. The history of the area's development and its impact on the landscape may be related to the differences in vector density observed between the north and the south rural area. We have shown that at the beginning of the 20th century, the colonial government displaced the inhabitants of the north rural area towards the main road, and also that the south rural was uninhabited. Consequently, the north rural area has been exploited much earlier than the south rural area. The first waves of immigration were into the north area, where immigrants were settled near existing fields. The oldest and biggest settlement in the southern area, the Baoule hamlet called « Deux Côtes », was only created in 1977. In the southern area, contrary to the north, patches of both relict forest and uncultivated lowland remain, being favourable breeding areas for tsetse flies. The risk of trypanosome transmission is not, however, absolutely correlated to vector density, but depends also on a number of contextual factors [18, 19] including human mobility. The track which goes to the south-east of Bonon is the most used, and goes through an environment favourable to the human-vector contact (edge of uncultivated lowland/plantations, edge of forest/communication routes) . The transmission of HAT in this area is thus likely to be due to the high density of tsetse flies combined with a high human attendance, in an environment favourable to the human-vector contact. The lack of movement between the north and south is likely to be the main reason to explain that the disease spreads from the south towards the town, but does not spread onward into the densely inhabited northern rural area . This area is thus characterized by a very low presence of vector and parasite, in an environment unfavorable to the human-vector contact, and the chance of transmission is thus too low to enable the development of HAT.
In the focus of Bonon, the history of human settlement has apparently determined to a great extent, both current land cover patterns and the prevailing density of tsetse flies which in turn explain the spatial distribution of HAT. This sequence of events is likely to have happened in other foci within Côte d'Ivoire. Other factors remain, that could not be included in this study but which could also play an important role, such as the presence/absence of reservoir animals, feeding habits of tsetse, the evolution of landuse regarding the socio-political events that have recently occurred in Côte d'Ivoire.
In common with other studies, this work highlights the value of a GIS analysis in the context of multidisciplinary approach, to gaining an understanding of the distribution and spatial dynamics of the disease, and the necessary conditions for effective prevention, notably in Africa . This work, by locating the most active transmission area at the south-east of the focus of Bonon, and by identifying the area with few disease cases, also helps to delineate the boundaries of the focus of Bonon more accurately. Targeted actions of tsetse control starting from north of Bonon (with little chance of tsetse reinvasion due to very low densities) to south, and targeted additional medical surveys in the south will be proposed to the Ivoirian HAT program, in order to reduce sleeping sickness in this area. The methodology used in the present work may be used in other areas of Côte d'Ivoire with similar history and similar environment to predict areas of possible sleeping sickness development/extinction. However it is likely that the current socio-political conditions in Côte d'Ivoire will have an impact on the further spread of HAT, on local, national and even international scales, particularly if forced movements of populations continue to occur .
Study area, presentation and description
The town of Bonon (7°N-6°W) is located about sixty kilometers west of the political capital of the country, Yamoussoukro (figure 1), in the Gouro ethnic group area,. The climate is equatorial with an annual rainfall of around 1 200 mm, and slight annual variations of temperatures (3°C). This region of the Central West Côte d'Ivoire is known for its historical (Bouaflé, Daloa) and contemporary (Vavoua, Sinfra) foci of sleeping sickness, but the focus of Bonon is comparatively recent [13–23]. The town of Bonon was created during the French colonial administration, when populations were forced to settle along communication routes, in order to have direct access to the labour necessary to the development, the maintenance and the exploitation of the area. In the early 70's, Bonon was a big village of agricultural labour immigrants, it has now become a commercial and administrative town (sub-prefecture of Marahoué region) of about 20 000 inhabitants. It is surrounded by villages, hamlets and encampments (with an additional total of about 10 000 inhabitants), representing more than fifty ethnic groups. Due to its infrastructure, Bonon has an important influence in nearby rural areas since the nearest urban centers (Daloa, Bouaflé, Sinfra) are located more than 30 kilometers away.
A total of 290 Vavoua traps  were set up on each patient's place of residence, water supply sites and working places- with the aim of obtaining data on the vectors distributions in relation human presence. Apparent Density per Trap per day (ADT: number of tsetse flies caught per trap and per day), infection by Trypanosoma brucei (the pathogenic parasite) using molecular tools (see below), and number of bloodmeals taken from humans were monitored. In the northern part (almost free of disease), traps were set up in areas the patients frequented. Each trap remained in place for four days, with cages being changed daily, and fly counts, sex-ratio determinations, and dissections being carried out daily. Tsetse flies (G. palpalis) were dissected to look for trypanosomes in the mouthparts, midgut, and salivary glands. Each organ (mouthparts, salivary glands, midgut) was put into a separate eppendorf tube containing 30 μl sterile distilled water for subsequent molecular analyses. Trypanosoma brucei identification was done by molecular analysis (PCR, polymerase Chain Reaction) using specific primers . In order to assess levels of contact between human and tsetse, the bloodmeal origin was assessed using the method of Diallo et al. . This method, based on variation of the Super Oxyde Dismutase (SOD) enzyme, distinguishes between bloodmeals taken from humans and animals.
Historical settlement of study area
Five administrative workers and several community leaders (religion, ethnic groups, youth) of town of Bonon and villages were interviewed, alternatively using individual or collective (around 20 people) discussions, in order to understand the history of the progressive settlement in this area. These interviews took place after several preliminary meetings in which the aim of the work was explained, in order to avoid any confusion due to the special context which prevailed in Côte d'Ivoire at the time of the study (March to May 2004). An additional objective was also to understand the evolution of the relationships between the different communities.
Two transects were carried out on foot (figure 4), one in the northern rural area of Bonon, the other in the southern rural area. The lines of these two transects were defined according to several parameters:
- Analysis of satellite image (Landsat 2000) covering the study area, which was used to determined landscape discontinuity.
- Knowledge of the area, acquired during the multiple travels by car and motorcycle.
- Where the patients lived.
These two transects were each 7 kilometers long. Landscape characteristics were assessed at points 250 metres apart using a description form, on which Global Positioning System (GPS) coordinates, landscape details, principal cultivation types and the names of the principal plant species were recorded. The data obtained were used to draw up a thematic classification of landscape, which was then extrapolated to the whole study area by the signal processing of Landsat 2000 satellite image. This signal processing was done under ENVI 3.2 (Environment for Visualizing images) software.
We defined six counting points (figure 5) on the principal tracks which link Bonon to the surrounding rural areas. At each of these points, every individual going from Bonon to the rural area and from the rural area to Bonon, from 6 am to 7 pm, every day during one week was recorded. At the same time, a random subsample was asked to complete a questionnaire, in order to obtain more detailed information on the nature of their journeys (place of departure, place of destination, reason for travelling).
All the data were recorded in a linked data base under Access. The data were then imported into Arcview 3.2., which was used to execute the spatial queries.
We are extremely grateful to the Ivoirian HAT control program and to the team « THA et glossines » of Institut Pierre Richet for their help, and to the national and regional administrative authorities for their collaboration. This work was funded by IRD and SCAC (Service de Coopération et d'Action Culturelle) Abidjan. We thank very much Dr. W. WINT (Environmental Research Group Oxford, UK) for critical reading of the manuscript.
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