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Trente ans de lutte contre l’onchocercose en Afrique de l’Ouest. Traitements larvicides et protection de l’environnement

 | 
Laurent Yaméogo
, 
Christian Levêque
, 
Jean-Marc Hougard

Sélection d’articles du programme OCP / Selected OCP papers

Twenty-two Years of Blackfly Control in the Onchocerciasis Control Programme in West Africa

J-M. Hougard, L. Yaméogo, A. Sékétéli, B. Boatin et K.Y Dadzie

Texte intégral

1Twenty-two years after the launch of the Onchocerciasis Control Programme in West Africa (OCP), Jean-Marc Hougard and colleagues critically review the vector-control strategy adopted. They go on to identify the few hydrological basins where transmission of the infection remains difficult to control, to analyse the causes and to propose appropriate corrective measures on a case-by-case basis. Most of these measures, which are mainly based on ivermectin chemotherapy, will continue to be applied after the end of the OCP in 2002, under the control of the countries concerned.

2Onchocerciasis, a dermal filariasis caused by Onchocerca volvulus, is a disease transmitted to humans by a blood-sucking dipterous insect, the blackfly (Simulium). The most serious manifestations are blindness and debilitating skin lesions. This disease is found in 37 countries, 30 in Africa, six in America and one in the Arabian península1. Africa is by far the most affected continent in terms of the severity of the clinicai manifestations of the disease and the extent of its distribution. Hence, as early as 1968, representatives of the Organisation de Coopération et de Coordination pour la Lutte contre les Grandes Endémies, WHO, Institut Français de Recherche Scientifique pour le Développement en Coopération (ORSTOM) and United States Agency for International Development, encouraged by the results of the pilot campaigns for the control of blackflies in the savanna zone of West Africa2, laid down the foundations of an ambitious regional onchocerciasis control project at a meeting in Tunis (1-8 July 1968).

3The Onchocerciasis Control Programme in West Africa (OCP)3 began its activities in January 1974. Its objective was to eliminate onchocerciasis as a disease of public health importance and as an obstacle to socio-economic development. The basic strategy was to interrupt the transmission of the blinding strain of O. volvulus for a period longer than the longevity of the adult worm in its human host (about 14 years)4. The interruption of transmission is achieved by destroying the larval stages of the vector, Simulium damnosum s.l., through the aerial application of selective insecticides to infested rivers (Fig. 1). Each week, the OCP selects the most appropriate insecticide (out of seven, which are used in rotation) for application in each river stretch to be treated (Fig. 1). This decision allows the optimization of larviciding in terms of cost-effectiveness, management of resistance and environmental protection5-6; several criteria need to be considered, not only relating to the insecticides, but also to the hydrological conditions and blackfly populations involved. One of the seven insecticides is a liquid concentrate of a biological control agent, Bacillus thuringiensis H-14 (Ref. 7). Of the six Chemicals, formulated as emulsified concentrates, three are organophosphates (temephos, phoxim and pyraclofos), two are synthetic pyrethroids (permethrin and etofenprox) and one is a carbarnate (carbosulfan).

4The first aerial insecticide treatments began in February 1975, in areas where the incidence of blinding onchocerciasis was highest. Later, the area covered was gradually extended to 654000 km2, spread over seven countries (Burkina Faso, south-eastern Mali, south-western Niger, the northern parts of Côte d'Ivoire, Benin, Ghana and Togo) by the end of 1977. However, it soon became apparent that the border of this area was infiltrated by infective blackflies originating from regions outside the OCP area8. To give permanent protection in the original OCP area and to control the vector in the basins where the re-invading Simulium originated, the hyperendemic regions were identified and larvicidal treatment was given9. This resulted in two extensions to the original OCP area, one to the west, comprising the basins of south-eastern Guinea and northern Sierra Leone (western extension), and a second to the south and east, comprising the southern basins of Côte d'Ivoire, Benin, Ghana and Togo (south-eastern extension) (Fig. 1).

5The installation of vector-control operations in the extension areas was completed towards the end of the 1980s, while all the basins of the original area were still being treated. The larviciding coverage then reached its peak with>40000 km of river being treated over an area of 106 km2, over nine countries of the OCP The satisfactory results achieved mean that larviciding operations have now stopped in almost all the basins of the original area. In the extension areas, larviciding is proceeding, and is combined with the distribution of the microfilaricide ivermectin, the only drug available so far which is suitable for the mass treatment of onchocerciasis10. By pursuing this combined drug and vector-control strategy, the whole of the basins treated should be free from onchocerciasis10. By 2002 at the latest, which is the end point of the OCP operations11. A few residual foci of infection will remain, however, after the conclusion of the OCP, both in the controlled areas and in the extension areas.

Residual foci in the original area

6The control strategy. The original OCP area is a savanna zone and is relatively homogeneous in its blackfly species and parasite strains. Before the OCP was launched, the area was plagued mainly with the most severe form of onchocerciasis, the savanna type, which is characterized by high blindness rates, and is transmitted by the group of savanna species of the S. damnosum complex (Fig.1)12-14. In principie, the vector-control strategy was simple to implement, as it consisted of arresting transmission of the parasite regardless of its pathogenicity, through the indiscriminate elimination of vector species15. Although the blackflies could carry animal filariae, some of which could not be differentiated from O. volvulus, evaluation of the treatments posed no particular problem. Indeed, the savanna blackflies were largely anthropophilic, and the annual transmission potential (ATP; Fig. 1) reflected the intensity of the blinding form of human onchocerciasis16.

7The implementation of this control strategy made it possible to interrupt transmission of the blinding strain of the parasite. From 1990, the first decisions to stop larviciding were made for the basins in which the situation was deemed satisfactory from both the epidemiological and entomological points of view17 18. Subsequently, vector-control operations ceased in other basins that had received at least 14 years of larviciding and where the trends of the epidemiological data indicated depletion of the parasite reservoir. However, because of contamination by infective blackflies, some rivers at the edge of the original area continued to be treated beyond the theoretical period of 14 years, and up to the time the extension areas were set up. Onchocerciasis is no longer a public health problem in the whole of the original area, that is, clinical signs of the disease have totally disappeared. WHO forecast in 1991 (Ref. 19) that the whole of the original area would be free from onchocerciasis by 1997; however, a few basins remain slightly endemic20

8The residual foci. The persistence of some residual foci is a cause for concern. While the risk of contamination of the adjacent basins remains, there is no guarantee that an alternative control strategy would succeed fully where the current strategy has only been a partial success. The OCP and the participating countries are therefore paying particular attention to these foci in an attempt to identify the factors that have hindered success. To our knowledge, six residual foci of onchocerciasis remain in the original area; a succinct analysis of these foci follows.

9(1) In the north-eastern part of Benin, a few villages located near two tributaries on the east side of the river Niger are still hypoendemic despite 18 years of uninterrupted vector control. The persistence of this focus is due to a seasonal contamination by infective blackflies carried by harmattan winds from untreated hyperendemic areas of Nigeria.

10(2) The problem of the Lower Black Volta focus in Ghana is partly caused by demographic factors. A recent sociological study21 has shown that this area attracted large numbers of migrants in search of new farmlands; the migrants mainly originated from areas to the east of Lake Volta, which were still endemic.

11(3) The control programme in the White Volta focus in Ghana was hampered for many years by serious logistical problems related to the inaccessibility of two of its tributaries during the rainy season. Some larval breeding sites thus escaped larviciding, allowing an unsuspected transmission to continue as a result of the inappropriate location of one blackfly-catching point.

12(4) In the Dienkoa focus in Burkina Faso, onchocerciasis remains mainly because of the premature decision to stop vector-control operations in the 1980s. This was partly a consequence of continuing undetected transmission as a result of an inappropriate reduction in the evaluation network.

13(5) The decision to stop larviciding in the basin of the Bougouriba, Burkina Faso in 1989 might also have been premature. Indeed, although transmission had been successfully controlled for more than 14 consecutive years, focal entomological, epidemiological or demographic signs suggested that larviciding should have been continued or, at least, some backup measures (entomological and / or epidemiological monitoring or ivermectin distribution) instituted.

14(6) Lastly, the causes of the persistence of high transmission levels and poor epidemiological results on three of the tributaries within the Oti focus are difficult to determine, but could result from interactions between climatic, demographic and logistical factors. Aerial larviciding, in combination with ivermectin treatment, is being continued pending further investigations.

15The corrective measures. The identification of the characteristic features of these foci has made it possible to take corrective actions, in particular, treatment with ivermectin and, to a lesser extent, larviciding. In the White Volta focus, considering the delay in controlling transmission and the fact that transmission is localized, the large-scale ivermectin treatment that was instituted in 1995, soon after larviciding was stopped, might accomplish more than a simple control of morbidity through more focal treatment. The relatively isolated nature of this focus and its low endemicity level, combined with the treatment regime employed (150 μgkg-1 twice a year), permits hope that a significant impact on transmission might be achieved, as occurred in the savanna zone of northern Cameroon22. In the Dienkoa focus, satisfactory larvicidal treatments, combined with ivermectin distribution, were achieved (ATPs <100 infective larvae per person per year, and no new infections in humans) only from 1990. The ground larviciding by health service technicians in Burkina Faso should end in 2001, after a period of 12 years of successful control, which is long enough to reduce the risk of recrudescence to <1%. In the Oti focus, where vector control is planned only until 2002, and in the other remaining foci, the long-term control of morbidity through community-directed treatment with ivermectin is probably the only remaining solution in the absence of a macrofilaricide suitable for mass treatment. Community-directed ivermectin treatment, which is used by the African Programme for Onchocerciasis Control, directly involves the exposed communities23, which is probably the best way to ensure optimal and sustainable protection of the populations after the conclusion of OCP, in the current socioeconomic context.

Potential residual foci in the extension areas

16History of onchocerciasis control. Larviciding of the river basins that were the initial sources of invasion by infective savanna blackflies commenced as early as 1979 in Southern Côte d'ivoire9. Year-round larviciding was started in 1987 in the Southern parts of Ghana, Togo and Benin, which were the sources of invasion to the Southern borders of the original area24, 25. In 1989, insecticide treatment of the basins of eastern Guinea and then, in 1990, those of northern Sierra Leone was started26, 27. With the registration of ivermectin in 1987, these basins also benefited from large-scale ivermectin treatment from 1989. This strategy led to a rapid reduction in ocular morbidity28 from the effects of ivermectin, as well as a longerterm reduction in transmission from the combined effects of ivermectin treatment and larviciding29. At the same time, the foci of Guinea Bissau, western Mali, Senegal and Southern Sierra Leone were treated with ivermectin only, because they were isolated, had low-level endemicity and were not a source of invasion into the original area. Thus, at the beginning of the 1990s, vector control and/or ivermectin treatment had brought blinding onchocerciasis under control over the entire area of almost 1 300 000 km2 of the 11 countries of the OCP (Fig. 1).

17The control strategy. In the extension zones undergoing larviciding, the nature of the soil, the altitude, latitude, rainfall or human activities determine the different types of vegetation, which range from the savanna in Sudan and Guinea to the degraded forests. This diversity is reflected in the habitats of different cytospecies of the S. damnosum complex, from the savanna to the forest vectors30. When larvicidal treatments were initiated, a selective strategy exclusively targeted at the savanna blackflies was considered. Flowever, the transmission dynamics of different parasite strains was unknown, and it was difficult to identify the infected adult females accurately. This option was therefore discarded in favour of a less targeted strategy, which took into account the seasonal abundance of the savanna blackflies in their larval habitat based on the cytotaxonomic tools available31. Species identification by cytotaxonomy is based on the analysis of the banding sequence on the polytene chromosomes from the larval salivary glands12. Among the nine sibling species of the S. damnosum complex found in the area covered by the OCP13, six are the primary vectors for O. volvulus in West Africa. Simulium sirbanum and S. damnosum s.s. are the primary vectors in the savanna, while S. squamosum and S. yahense are the primary vectors in the rain forest. The remaining two vector species, S. leonense and S. sanctipauli, have a restricted distribution, which is mostly limited to the large Coastal rivers of Sierra Leone and Côte d'ivoire, respectively30.

18Morphological identification of adult blackflies has now improved, allowing the differentiation of the savanna species from the others at the same blackfly-catching point30. DNA probes can differentiate between the savanna strain and the forest strain of the parasite32, and a technique involving mitochondrial DNA sequences is being developed, which allows the identification of the adult flies of the six main vector species33. These methods are providing insights into the mechanisms of transmission under natural conditions and, hence, into vector-control strategies. Toé and colleagues34 have shown that the relation between savanna vectors and the blinding strain of the parasite is not as clear as was suggested by earlier experimental xenodiagnostic studies. The consequent overemphasis on the role of savanna species in transmission, when planning control activities, might favour the transmission of blinding onchocerciasis by the forest blackflies. This hypothesis is supported in that the vectorial capacity of forest species is higher than that of savanna species35. However, other observations made in several basins of the extension areas suggest that the current strategy can be maintained without jeopardizing the achievements of vector control. For example, at the Benin village of Kaboua in the degraded forest zone (Fig. 1), transmission of the savanna parasite strain is relatively high (an ATP of 421 infective larvae per person per year in 1996), although the transmission is mainly due to forest blackflies originating from the untreated basins of Nigeria (S. soubrense Beffa type)36. This level of transmission, in the savanna zone, would have been assodated with clinicai signs.

19These different observations underline the uncertainties regarding the threat posed by the blinding strain of the parasite in the extension areas. Research is now under way to improve molecular tools (heteroduplex, DNA microsatellites) to facilitate the identification of the vector and parasite populations33,37. The heteroduplex technique permits the identification of individuais on the basis of hybridization with mitochondrial DNA fragments. Microsatellite DNA provides useful polymorphic markers for populations and even for individuals. The application of immunodiagnostic techniques to determine whether different levels of pathogenicity exist in the parasite or whether individuals can be predisposed to develop blinding onchocercal lesions is also being planned. Pending the results of these studies, with five years to go to the end of larvicide treatments, the current vector-control strategy – a realistic compromise between a selective option and a more global option – should be pursued without major changes until the conclusion of the OCP.

20The potential residual foci. Vector control, combined with ivermectin distribution, is being continued in almost all the basins of the extension areas. Larviciding is planned to stop at the end of 1998 in the Côte d'Ivoire basins, and between 2001 and 2002 in the western and south-eastern extensions38,39. However, in a few river basins where the blinding strain of the parasite predominates, transmission sometimes remains difficult to control despite continued larviciding and the distribution of ivermectin (eg. the Lower Tinkisso, Guinea, in the western extension, and the Pru, Ghana, in the south-eastem extension). Therefore, as observed in the original area, it is possible that a few residual foci of savanna onchocerciasis will persist after the end of the OCP. After 2002, when vectorcontrol measures will have ceased, in the absence of a macrofilaricide suitable for mass treatment, ivermectin will be the only means of control for these residual foci. The research mentioned previously, if successful, will help to assess the threat represented by these foci, allowing the appropriate adjustment in ivermectin-treatment strategies on a case-by-case basis. Meanwhile, work on modelling onchocerciasis transmission and its control might help to determine precisely how long ivermectin distribution needs to be continued to make the recrudescence of blinding onchocerciasis unlikely40

Fig. I. An OverView of the vector-control activities in the Onchocerciasis Control Programme in West Africa (OCP). The map (top left) shows the different operational phases of the OCP and identifies the residual foci in the original OCP area. The photograph below (kindly supplied by the Institut Français de Recherche Scientifique pour le Développement en Coopération) shows an adult of Simulium damnosum s.l. complex species, which is responsible for the transmission of onchocerciasis. The background shows a helicopter (photograph kindly supplied by OCP) spraying one of seven larvicides selected according to their operational range (bottom right). In this figure, the position of the fish represents the minimum level of water discharge with respect to the water gauge at which the product is authorized to be used because of the risk of impact on the environment The dollar sign ($) represents the level above which the cost of use of the product is no longer acceptable. The entomological evaluation is also shown (bottom left). The entomological index most frequently used to quantify transmission is the annual transmission potential (ATP): the theoretical number of infective onchocerca larvae that a person at a catching point would receive if highly exposed to blackfly biting 12 hours a day for 12 months a year. In the savanna area, transmission of onchocerciasis at a level <100 infective parasite larvae per person per year is considered to give no risk of developing severe ocular lesions.

Transfer of residual activities

21By 2002, the responsibility for maintaining the residual activities of the OCP will be transferred to the participating countries. A few residual foci will remain in both the original and the extension areas; however, their total size will be fairly small compared with the 25 million hectares of fertile land that will be disease free by the end of the OCP; furthermore, the disease will no longer be a public health problem. Although the studies conducted so far in the disease-freed zones have given encouraging results, it is possible that new onchocerciasis foci will emerge after 2002 in the areas currently considered to have been freed. In the basins of the White Volta in the southeast of Burkina Faso, for example, onchocerciasis has been reduced from hyperendemic to almost absent after 14 years of vector control alone. The latest parasitological surveys still show excellent results six years after larviciding was stopped.

22The health services of the countries involved must be given the means to detect an onchocerciasis focus early enough that control is feasible. The necessary tools and know-how for entomological surveillance will be made available by the OCP to the national health services to enable them to detect a resurgence of transmission. A simple and cheap method for the detection of infective larvae of the parasite in blackflies is in the process of being tested for use in the field41. This method will provide an early warning of potential recrudescence, enabling the health services of the affected area to apply the various techniques currently available or in development42 before the infection becomes difficult to control. In the Southern areas of the OCP, especially south-eastem Côte d'Ivoire, south-eastem Guinea and south-western Ghana, the national health services will also have to monitor closely the consequences of deforestation on vectorial dynamics and, hence, on the epidemiology of onchocerciasis. For the time being, to avoid any deterioration of the situation, OCP will provide the countries with logistical and technical support for the distribution of ivermectin to control onchocercal morbidity, regardless of pathogenicity.

23All vector-control activities will probably have ceased by the end of 2002, as sustained vector-control action to arrest transmission in each residual focus would be beyond the budgets of the participating countries. However, the use of ground larviciding with non-toxic and non-persistent insecticides to control blackfly nuisance might increase, at least in socio-economically important sites, where the efficient and sustainable management of such treatments is possible43

Acknowledgements

24The authors dedícate this article to the late Daniel Quillévéré, Chief of the Vector Control Unit at OCP 1989-1994. They thank most sincerely B. Philippon, former Chief of the Vector Control Unit and Head of the Health Department of ORSTOM in Paris, David Molyneux, Chairman of the Expert Advisory Committee of OCP and Director of the Liverpool School of Tropical Medicine, UK, and A.W. Soumbey from the OCP, who participated in the revision of this paper and encouraged its publication. Sincere thanks are also extended to the entire technical and administrative staff of the OCP, especially in the Vector Control Unit and in the entomological, hydrological and hydrobiological national teams, who have contributed to the success of the OCP from 1974 to the present.

Bibliographie

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Légende Fig. I. An OverView of the vector-control activities in the Onchocerciasis Control Programme in West Africa (OCP). The map (top left) shows the different operational phases of the OCP and identifies the residual foci in the original OCP area. The photograph below (kindly supplied by the Institut Français de Recherche Scientifique pour le Développement en Coopération) shows an adult of Simulium damnosum s.l. complex species, which is responsible for the transmission of onchocerciasis. The background shows a helicopter (photograph kindly supplied by OCP) spraying one of seven larvicides selected according to their operational range (bottom right). In this figure, the position of the fish represents the minimum level of water discharge with respect to the water gauge at which the product is authorized to be used because of the risk of impact on the environment The dollar sign ($) represents the level above which the cost of use of the product is no longer acceptable. The entomological evaluation is also shown (bottom left). The entomological index most frequently used to quantify transmission is the annual transmission potential (ATP): the theoretical number of infective onchocerca larvae that a person at a catching point would receive if highly exposed to blackfly biting 12 hours a day for 12 months a year. In the savanna area, transmission of onchocerciasis at a level <100 infective parasite larvae per person per year is considered to give no risk of developing severe ocular lesions.
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Auteurs

At the Institut Français de Recherche Scientifique pour le Développement en Coopération (ORSTOM) and is seconded to the World Health Organizaron, currently based at the Vector Control Unit of the Onchocerciasis Control Programme in West Africa (OCP), PO Box 549, Ouagadougou. Burkina Faso. Laurent Yaméogo, Azodoga Sékétéli, Boakye Boatin and Kofi Yankum Dadzie are at the OCP. A. Sékétéli Is also the Programme Manager for the African Programme for Onchocerciasis (APOC). Tel: +226 34 22 57, Fax: +226 30 21 47, e-mail: hougard@oncho.orstom.bf

© IRD Éditions, 2003

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