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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

Environmental Assessment of Larvicide Use in the Onchocerciasis Control Programme

D. Calamari, L. Yaméogo, J-M. Hougard et C. Lévêque

Texte intégral

1The objective of the Onchocerciasis Control Programme (OCP) is to eliminate onchocerciasis as a disease of public importance and as an obstacle to socio-economic development. The OCP was initially based solely on the control of the blackfly vector, Simulium damnosum sensu lato, by insecticide spraying of the breeding sites on river Systems, where larval stages develop. Results of monitoring the environmental effects and the process of risk assessment for new insecticides are reviewed. The achievements of this strategy are outlined here by Davide Calamari, Laurent Yameogo, Jean-Marc Hougard and Christian Leveque.

2Onchocerciasis (river blindness) is caused by a filarial worm Onchocerca volvulus; the microfilariae live in the skin and cause debilitating skin lesions and, ultimately, blindness. West Africa used to be the most affected area in terms of the distribution and severity of clinical manifestations of the disease. Since 1974, successful control has been undertaken through the Onchocerciasis Control Programme (OCP)1-3.

3The strategy of larviciding is designed to interrupt the transmission of the parasite for longer than the longevity of the adult worms in a human host (estimated to be ~14 years) by destroying larval stages of the vector through aerial application of insecticides at breeding sites. The development of the aquatic stage from egg to pupae is around one week, hence insecticide application is undertaken weekly. At the peak of larviciding activities, during the years 1986-1991, ~50 000 km of river were treated in an area of over 1 000 000 km2.

4Recently, the introduction of a microfilaricide (ivermectin) for mass chemotherapy suggests that the combined use of ivermectin and larviciding should reduce the required duration of vector control to 12 years4. Despite the introduction of ivermectin, and in the absence of a macrofilaricide, vector control remains the method of choice to achieve the goals of the OCP5

5Because prolonged and regular use of insecticides presents a potential risk to the aquatic environment, an ecological group was set up, prior to launching the OCP, in order to: (1) organize a long-term monitoring programme of the aquatic fauna; (2) identify criteria for the selection of pesticides for operational use, and determine the conditions by which insecticide use can be optimized in relation to season and environmental factors in different areas of the OCP; and (3) review the nature of the agricultural development process being undertaken and proposed in the areas liberated from onchocerciasis, and identify the environmental and human ecological implications of such development.

6Although methods, procedures and protocols for the monitoring and risk assessment programmes have evolved since 1974, with the OCP responding to continually changing situations (insect re-invasion, resistance, variability in hydrology, etc.), basic concepts remain. The monitoring activities conducted by National Hydrobiological Teams and the ecotoxicological research carried on by the Hydrobiological Unit of the OCP, which also coordinates and assists the field work in the OCP area, are reviewed annually.

7The criteria for the evaluation of insecticide impact on aquatic environment include: (1) the vector control activities should not reduce the number of invertebrate species, or cause a marked shift in the relative abundance of species; (2) the pesticides applied should have neither a direct impact on fish, nor an effect on the life cycle of fish species; (3) bioaccumulation and biomagnification through food webs should be avoided; (4) human activities in the control area should not be impaired; and (5) temporary and seasonal variations in non-target invertebrate populations are acceptable.

8A network of sampling stations exists throughout the OCP area where selection criteria have been met6. Initially, there were 40 sampling sites, but as the programme evolved together with the treatment strategy, the number has been reduced to ten for invertebrates and ten for fish (Fig. 1).

9Details of the methods and sampling techniques for OCP monitoring programmes have been described7-9. It was realized, however, that information on the biology of the aquatic fauna in West Africa was generally limited, and so specific studies were undertaken to provide ecological baseline information.

Vector control

10Vector control has faced three major obstacles5. (1) It was established that the border of the initial area (654 000 km2 spread over seven countries) was invaded by migrating infective blackflies originating from outside the designated area. To protect the core area, vector control was extended (between 1986 and 1990) in the west and southeast, with two additional countries joining the OCP. (2) Five years after the beginning of the OCP, resistance of Simulium damnosum to temephos was detected10. This organophosphorous compound, the only insecticide used at the beginning of the programme, was selected because of its efficacy, its carry (distance over which it remains effective), its limited impact on non-target fauna and also its acceptable cost. After the development of insect resistance to another organophosphate (chlorphoxim) was detected, the OCP adopted a strategy of rotational use of different classes of insecticides, with different modes of action, to prevent development of further resistance. (3) Seven insecticides are currently used5: six of them formulated as emulsifiable concentrates (temephos, phoxim, pyraclofos, permethrin, etofenprox and carbosulfan), while the seventh is a liquid concentrate of a biological insecticide, Bacillus thuringiensis H-14 (Bt-14). The rotational use of insecticides has been particularly effective, with only limited resistance to the organophosphates currently in use, while the susceptibility of the Simulium populations to other classes of compounds remains unchanged.

Fig. I. Onchocerciasis Control Programme (OCP) area and location of invertebrate and fish monitoring stations.

11The consideration of environmental concerns has resulted in a number of limitations and restrictions in the use of the available insecticides for the rotational vector control.

Invertebrate and fish monitoring results

12For the monitoring process, invertebrate data have been collected in each river and analysed independently, distinguishing, for each river, the three types of sampling technique adopted. Invertebrates collected directly from the river-bed by means of a Surber net (named invertebrate community, living exactly at the sampling station), day and night drift, where the nets capture animals transported by water (named invertebrate assemblages, which include organisms from upper river locations).

13Numerical analysis methods to assess the variations in invertebrate community structure during the periods of treatment and during the periods when larviciding is suspended permit the evaluation of two principal properties of the biological communities: (1) their resistance (capacity of contrasting stress factors); and (2) their resilience (capacity to recover after stress).

14The taxonomic levels as well as the functional feeding group (trophic role) of the invertebrates sampled have been determined; the analysis of the biological variation has been focused on these structural and functional attributes. The OCP concern is to prevent the loss of faunal biodiversity, and to maintain the quality of the biomass available for the higher trophic levels in the food webs, while conserving the stability of the energetic flows (quantity). As the invertebrate communities represent lower levels of the aquatic food webs, any change can be a signal of potential detrimental effects on the ecological characteristics of the whole river System.

15On the basis of preliminary results, the following analyses were undertaken: (1) invertebrate taxonomic diversity; (2) relative abundance of functional groups; (3) rank abundance models; and (4) multivariate analysis11.

16The taxonomie diversity indices calculated during pretreatment periods showed a normal structure of invertebrate communities. The result was obtained from relative abundance of functional groups and diversity indices and from rank abundance models.

17During separate insecticide treatments, some rivers showed only limited changes in invertebrate community structure; in others, great changes occurred.

18Individual larvicides have different impacts on river fauna, depending on the river System to which they are applied. Moreover, each insecticide shows a characteristic distribution of effects on various invertebrate taxa, thereby providing a 'fingerprint', because of selective action on particular groups of insects, according to the mode of action of different types of larvicides12.

19Rotational use of the larvicides has led to difficulties in interpreting some biological data because of the additional effects related to previous treatment history. This is most frequently seen during a period of suspension, when the invertebrate recovery is related to the type and the severity of the stresses that occurred during past treatments.

20A first survey of the impact of the larviciding campaign was made after the initial phase of the programme, when only temephos, chlorphoxim and Bt-14 were applied. This demonstrated an initial deleterious impact on non-target fauna during the first year (limited reduction in biomass and number of taxa). However, not-withstanding the continuation of the treatments, there was a partial recovery within a year. Long-term studies (several years) showed such types of insecticides had little impact6,7.

21A recent evaluation of 20 years of OCP monitoring data11,13, for a period when different groups of Chemical substances (eg. carbosulfan and permethrin) were used, showed greater effects of the insecticides on the invertebrate fauna, particularly the rarefaction of a few taxa and, for example, in the case of permethrin, a biomass reduction. However, the ability of the aquatic biota to recover was demonstrated, even if, at a slow rate. Therefore, the taxonomic and functional variability in non-target invertebrate fauna seems to be compatible with the range of biological variation that would normally occur in these river Systems11,13.

22In the normal situation, invertebrate communities are rarely constant in taxonomic and trophic composition because of natural stresses (eg. unusual hydrological conditions, such as drought and spate events), which occur frequently. When these factors are taken into consideration, the 'biological variations previously discussed are ecologically acceptable': a conclusion confirmed by analysis on fish monitoring14,15.

23Fish populations at most monitoring sites show no evidence of a reduction in species richness after almost 20 years of larviciding in the original area of the programme, and seven years of larviciding in Guinea15. In an earlier evaluation6,16, the same conclusions were reached after ten years of larviciding with temephos, chlorphoxim and Bt H-14. Although the total number of species could mask changes in species composition, results from all rivers showed no loss of species after 20 years of larviciding.

24Fish catches per unit of effort (ie. a standard time during which nets remain in the river) with a standardized set of gill nets has demonstrated a seasonal pattern, with high catches at the low water period (January – April) and lower catches in the wet season (August – November). Long-term, yearly fluctuations are well correlated to the hydrological pattern, as has been observed for African rivers17.

25The coefficient of condition, a ratio between weight and length (corpulence), of the principal species of fish fluctuates around the expected means, which have not changed significantly during the programme. This suggests that larviciding has no effects on food availability, and that the feeding habits of fish have not altered18.

26There has, therefore, been no evidence of fish mortality due to larviciding at the operational doses in the OCP area. However, fluctuations have been observed in the abundance of biomass and richness of fish species. These variations are correlated to hydrological patterns, and can also be attributed to the pressure exerted by local fisherman, in certain areas.

27As a result of the first ten years monitoring the use of organophosphate insecticides and Bt-14, the Ecological Group decided to reduce the number of monitoring stations, and to change monitoring strategies by abandoning drift-sampling19.

28Moreover, during the annual evaluation of the research on new insecticides (see below), and as derived from monitoring data, several means of reducing the impacts of new Chemicals have been suggested. The following proposals have been made: (1) temephos and Bt-14 are considered as harmless for the environment and can be used without restrictions; (2) pyraclofos might show some toxicity (for example, in an accidental overdose) against the non-target fauna, particularly fish, and it is recommended that it be used at discharges above 15m3 s-1 but without any restriction on the number of cycles; (3) permethrin and carbosulfan should only be used above 70m3 s-1 and (if possible) for not more than six weeks per year on the same stretch of river; and (4) although the toxicity of etofenprox for fish and crustaceans is less than permethrin, its utilization should remain limited to discharges above 15 m3 s-1 but without any restriction on the number of annual cycles.

29For these reasons, the OCP has established a satellite transmission network for recording water discharge, allowing for in-time management of hydrological data in the treatment of the rivers20.

Risk assessment for new larvicides

30In addition to the above monitoring activities, the OCP has carried out a number of ecotoxicological studies on candidate larvicides.

31Acute toxicological tests have been performed on African fish species according to standard protocols21 to obtain original data on fish toxicology. Short-term impact on non-target invertebrates was also studied using a System of artificial gutters (semifield equipment). Qualitative and quantitative drift in such Systems have been evaluated at different concentrations, including the operational dose, and the larvicides classified according to their general toxicity and the typology of the susceptibility of the principal taxa established22-23.

32Bt-14 has proved to be the most selective and the least environmentally damaging larvicide of the seven. The other insecticides can be classified as follows, in increasing order of toxicity: temephos, chlorphoxim, pyraclofos, etophenprox, permethrin and carbosulfan.

33Among the taxa studied, the Baetidae were the most susceptible to the Chemical larvicides. The Hydropsychidae were fairly susceptible, while the Chironomidae were the organisms least susceptible to most of the insecticides. Results suggest that the more toxic the insecticides were in gutter tests, the more the population abundance differed from the reference ones in the field.

34A risk assessment in different steps was performed for every new larvicide to be used in the OCP. After the first trials, where efficacy on blackflies was evaluated (as well as physical properties such as dispersion and viscosity), a review of the literature was performed, together with some laboratory tests on fish, and gutter tests on invertebrates. The Ecological Group reviewing the results recommended, in cases of acceptable toxicological results, small-scale pilot studies in the field, with spraying to be carried out a few meters upstream of the evaluation zone.

35For the most toxic insecticides that have many advantages to their possible use (such as low cost, wide range of applications in relation to discharges and long carry distance), large-scale studies below the operational dose were recommended. This allows a complete risk assessment scheme to be obtained24 before the insecticide is used as an operational larvicide. Permethrin, for example, was tested in this way25. After 15 weekly applications at its operational dose, benthic fauna density and diversity were severely affected. However, both drift and benthic fauna recovered almost to pretreatment levels a month after the treatment was terminated, but one taxa remains absent. Fish showed some evidence of stress, but remained in the treatment zone, allowing catches to be compared with those of the control station. No fish mortality was observed, nor any variation in the condition factors of the fish.

Fig. 2. Synopsis of the Ecological Group activities. Introduction of the operational insecticides and the different toxicity tests in the programme. Bt-14, Bacillus thuringiensis H-14 ; EIA, environmental impact assessment.

36All these studies have allowed the OCP and the Ecological Group to agree on the optimal use of larvicides that limits the environmental impact. A synopsis of the activities of the Ecological Group is shown in Fig. 2.

Environmental impact and development

37The success of the OCP in vector control in West Africa has allowed extensive areas of previously abandoned valleys to be resettled and developed.

38Thus, despite the long-term use of larvicides in the rivers of the OCP area, the quality of the aquatic environment has been preserved, largely because of the precautions taken, and because of the absence of human population pressure in the areas most severely affected by the illness. However, the situation is now changing rapidly, and there is an increasing concern for the aquatic and terrestrial environments, because of population movements and land recolonization.

39It was recognized, therefore, that there was a need for the formulation of an appropriate methodology for environmental impact assessment. A pilot project in the Upper Leraba Basin was launched in 1993, the primary objectives being: (1) to assess the present environmental situation in the basin, with a view to determining potential sources of impact on the aquatic environment; (2) to quantify Chemical loads and assess the modification to the physical environment; and (3) to identify simple study methods applicable to other areas, and investigate ways to minimize impacts.

40An evaluation of the changes in the physical environment was made for the period between 1972 and 1993. These studies showed that about 75% of the original savanna woodland had been cleared in the past few years for settlement and agricultural development. There had been no observed significant disturbance of the riverine forest and associated floodplain grasslands of the main rivers System, and organic loads and nutrients were only of relevance along limited stretches of the main Leraba River, where point sources of contamination can be identified (eg. human and cattle wastes).

41The presence in river water of pesticides used for cotton protection was calculated from the quantity of Chemicals used locally by means of simulation models, which permitted the concentrations of pesticides in the river to be estimated. Although the predicted concentrations of pesticides in river water were not at levels that would cause damage or give cause for alarm, they could nevertheless be considered as early warning signais26

Conclusions

42The OCP has repeatedly been able to demonstrate that, despite the weekly application of larviciding over a long period, there has been no significant deterioration of the aquatic environment.

43The resuit of the OCP activity should not only be regarded as a success in curbing and controlling river blindness, but also as an important example of Sound environmental management in a programme that, from the beginning, had included ecological considerations in planning vector control activities.

Acknowledgements

44The authors are grateful to the OCP Director Yankum K. Dadzie for support and encouragement, and to David Molyneux, Chairman of the Expert Advisory Committee, for his help and suggestions about the manuscript.

Bibliographie

References

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2 Webbe, G. (1992) The Onchocerciasis Control Programme. Trans. R. Soc. Trop. Med. Hyg. 86,113-114

3 Molyneux, D.H. (1995) Onchocerciasis control in West Africa: current status and future of the Onchocerciasis Control Programme. Parasitol. Today 11, 399-402

4 Plaisier, A.P. et al. (1997) The required duration of combined annual ivermectin treatment and vector control in the Onchocerciasis Control Programme in West Africa. Bull. WHO 75, 237-245

5 Hougard, J.M. et al. (1997) Twenty-two years of blackfly control in the Onchocerciasis Control Programme in West Africa. Parasitol. Today 13, 425-431

6 Leveque, C. (1989) in Ecotoxicology and Climate, with Special Reference to Hot and Cold Climates. SCOPE 38 (Bourdeau, P. et al., eds), pp 317-335, John Wiley & Sons

7 Yameogo, L. et al. (1988) Dix ans de surveillance de la faune aquatique des rivières d’Afrique de l’Ouest traitèes contre les Simulies (Diptera: Simuliidae), agents vecteurs de l'onchocercose humaine. Naturaliste Canadienne 115, 287-298 (in French)

8 Leveque, C. et al. (1979) The Onchocerciasis Control Programme and the monitoring of its effects on the riverine biology of the Volta River Basin. Limnol. Soc. Symp. Ser. 5, 133-145

9 Yameogo, L. et al. (1991) The aquatic monitoring and bioassay component of the WHO Onchocerciasis Control in West Africa. Verh. Int. Ver. Theor. Angew. Limnol. 24, 2932-2935

10 Guillet, P. et al. (1980) Mise en èvidence d'une rèsistence au tèmèphos dans le complexe Simulium damnosum (S. sanctipauli et S. soubrense) en Cote d'ivoire dans la Zone du Progamme de Lutte contre l'Onchocercose dans la Région du Bassin de la Volta. Cah. ORSTOM Sèr. Ent. Mèd. Parasitol. 17, 291-299 (in French)

11 Crosa, G. et al. (1998) Long-term quantitative ecological assessment of insecticide treatments in four African rivers: a methodological approach. Chemosphere 37, 2847-2858

12 Yameogo, L. et al. (1992) Typology of susceptibilities of aquatic insect larvae to different larvicides in a tropical environment. Chemosphere 24, 2009-2020

13 OCP/WHO (1997) Quantitative Ecological Assessment of 20 Years of Invertebrate Collections during Onchocerciasis Control Programme in West Africa, Internal Report OCP/WHO Ouagadogou

14 OCP/OMS (1997) Rèsultats de 20 Annèes de Surveillance Ichtyologique en Afrique de l'Ouest, Internai Report OCP/WHO Ouagadogou (in French)

15 Abban, E.K. et al. (1997) in African Inland Fisheries, Aquaculture and the Environment FAO/Fishing News Books (Remane, K., ed.), pp 136-149, Blackwell Science

16 Leveque, C. et al. (1988) Onchocerciasis Control Programme in West Africa: ten years of monitoring fish populations. Chemosphere 17, 421-440

17 Welcomme, R.L. (1985) River fisheries. FAO Fish. Tech. Pap. 262, FAO

18 Abban, E.K. and Samman, J. (1982) Further observations on the effect of Abate on fish catches. Environ. Pollut. (A), 27, 245-254

19 OCP/WHO (1987) Ecological Group Report of the Eighth Session, Bouakè, Internal Report OCP/WHO Ouagadogou

20 Servat, E. and Lapetite, J.M. (1990) Hydrologie, informatiqueet satellite, un renfort à la lutte contre l'onchocercose. ORSTOM Actualitès 29, 22-26 (in French)

21 Yameogo, L. et al. (1991) Laboratory toxicity of potential blackfly larvicides on some African fish species in the Onchocerciasis Control Programme area. Ecotoxicol. Environ. Saf. 21, 248-256

22 Yameogo, L. et al. (1991) Typologies des entomocènoses bentiques soumises à des èpandages d'insecticides antisimuliidiens. Arch. Hydrobiol. 123, 11-127 (in French)

23 Yameogo, L. et al. (1993) Short-term toxicity of pyraclofos used as blackfly larvicide on non-target aquatic fauna in a tropical environment. Chemosphere 27, 2425-2439

24 Calamari, D. and Di Guardo, A. (1993) in Chemical Exposure Predictions (Calamari, D., ed.), pp 169-185, Lewis Publishers

25 Yameogo, L. et al. (1993) Effects of permethrin as Simulium larvicide on non-target aquatic fauna. Ecotoxicology 2, 157-174

26 Baldry, D. et al. (1995) Environmental impact assessment of settlement and development in the Upper Lèraba Basin. World Bank Tech. Paper 302, The World Bank

Table des illustrations

Légende Fig. I. Onchocerciasis Control Programme (OCP) area and location of invertebrate and fish monitoring stations.
URL http://books.openedition.org/irdeditions/docannexe/image/28614/img-1.jpg
Fichier image/jpeg, 213k
Légende Fig. 2. Synopsis of the Ecological Group activities. Introduction of the operational insecticides and the different toxicity tests in the programme. Bt-14, Bacillus thuringiensis H-14 ; EIA, environmental impact assessment.
URL http://books.openedition.org/irdeditions/docannexe/image/28614/img-2.jpg
Fichier image/jpeg, 182k

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