Communities of practice
Impact Of Mass Drug Administration On Anopheles-Transmitted Filariasis In Africa: Emerging Data From Ghana And Mali
21 Jan 2008
1Health Research Unit, Ghana Health Service, Accra, Ghana
Working paper for the Scientific Working Group meeting on Lymphatic Filariasis Research, convened by the Special Programme for Research and Training in Tropical Diseases, Geneva, 10–12 May 2005
Full text source: Scientific Working Group, Report on Lymphatic Filariasis, 10–12 May 2005, Geneva, Swizterland, Copyright © World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases, 2005, http://www.who.int/tdr/publications/publications/swg_lymph_fil.htm
Recent evidence suggests that anopheline transmitted lymphatic filariasis can be eliminated worldwide because of the phenomenon of facilitation. This hypothesis indicates that, at low microfilaria densities, Anopheles vectors of filariasis are less efficient in transmitting Wuchereria bancrofti. This has been borne out by observations in Papua New Guinea where the vector is Anopheles punctulatus . However, it may not be practical to generalize this observation worldwide since the threshold levels of microfilaraemia needed for elimination of anopheline transmitted W. bancrofti lymphatic filariasis (LF) might differ from species to species [16–18]. For example, results from earlier studies in sub-Saharan Africa, on the quantitative relationship between transmission intensity and microfilarial reservoir, indicated variation among members of the An. gambiae complex and An. funestus [3,4,14].
In Ghana, several sympatric Anopheles species are vectors of Wuchereria bancrofti ; these species are likely to differ in their vectorial role and capacity to transmit low density microfilaraemia. For example, Appawu et al.  observed that no An. arabiensis (a member of the An. gambiae complex) was positive for W. bancrofti although this species formed 9%–14% of An. gambiae s.l. Furthermore, analysis of pooled data for Anopheles mosquitoes from a recent study by Boakye et al.  indicated presence of the ‘limitation’ process, although larger samples need to be investigated to determine whether this process occurs only in An. gambiae s.l. or An. funestus or in both of these taxa.
Although the impact of treatment on transmission of LF has not been studied in Ghana, there have been some transmission studies and investigations on the efficacy of different treatment regimes [1,9]. Concerning treatment efficiency, Dunyo and Simonsen  observed that re-treatment of Wuchereria bancrofti microfilaraemia with a combination of ivermectin and albendazole resulted one year later in an overall mean reduction in microfilarial intensity of 76.2%. The efficacy of the combination treatment thus appeared to be largely independent of the type of primary treatment given and was multiplicative when used repeatedly. Gyapong  evaluated the impact of a single dose of ivermectin in six communities in Ghana after two years (due to unavailability of the drug for re-treatment in the second year); this showed the community microfilaraemia prevalence and intensity to be reduced, respectively, by only 25.5% and 39.5% of pre-treatment levels.
Although LF has been known in Mali since 1912 , only a few studies have been aimed at determining disease burden and transmission patterns [13,20]. The data show, however, that the LF infection rate increases from the northern to the southern part of the country, and they confirm the nocturnal periodicity of W. bancrofti. Entomological data have identified the gambiae and funestus complexes as the main vectors of LF in Mali. Recently Coulibaly  reported a survey carried out 20 years after a previously reported study in the same endemic area (savannah area). The data show a significant decrease of infection rate in both human and vector in the absence of any control measures. Data from Keita  however, on the prevalence of elephantiasis in the country, show that LF is a major public heath problem in Mali.
The Ministry of Health (MOH) coordinating group undertook mapping of LF in eight regions of the country in 2002, and in Bamako, the capital city, in 2004 (supported by WHO). In the eight regions, the infection rate by the immunochromatographic card test (ICT) ranged from 1% in Timbuktu (northern part) to 18.6% in Sikasso (southern part) with a mean infection rate of 7.07% (n = 100 per community). In the capital city (six communes), the average infection rate was 1.5% (n = 5990); four communes were found positive using ICT.
The Lymphatic Filariasis Elimination Programme of the Ghana Health Service and the Malian MOH are undertaking elimination of LF using mass drug administration (MDA) with ivermectin and albendazole. The elimination programmes have been set up in both countries as part of the Global Programme to Eliminate Lymphatic Filariasis using the following strategies:
This provides the opportunity to investigate the impact of MDA on transmission by members of the An. gambiae complex and An. funestus group.
Current state of knowledge and available evidence on impact of MDA on transmission
These studies were organized as multicountry studies with the aim of evaluating the effect of community-based mass chemotherapy on the transmission of LF. The specific objectives were to:
In Ghana, the study sites included eight villages in a district with a record of filariasis endemicity where there had not been any community-wide treatment but which had been earmarked for treatment with ivermectin and albendazole. A census was carried out in all eight villages: all houses were enumerated and demographic data of the inhabitants recorded, including the use of bednets. In Mali, similar baseline data were collected using a common protocol.
Entomological studies (assessing transmission)
Each village was divided into four sections and one house per section selected randomly for overnight mosquito collection using the man-landing catch method. Four houses were sampled in each village per night (from July to December, from 2001 to 2004); the mosquitoes were later dissected in the laboratory.
Inhabitants surveyed for W. bancrofti infection were randomly selected by computer. The first prevalence survey was conducted during February 2002 before mass treatment of the inhabitants (in March 2002). Subsequent surveys were done in 2003, 2004 and 2005. Each time, the surveys preceded MDA in the communities.
The average coverage by MDA in the three years for the eight villages was around 66% (table 1). The lowest coverage was 13.9% in the village of Fawomanye in 2002; this situation improved to 62% and 65% in subsequent years (2003 and 2004, respectively). At the time of writing, treatment had been completed at all sites for 2005 and data were being collected.
Parasitological examination of blood smears has shown a decrease in proportion of positive individuals in the population. In 2002, the proportion was 4.6%; in the most recent survey, in January 2005, this had declined to 0.9% (fig. 1 and table 2).
Mean prevalence of microfilaraemia over a four-year period (Ghana)
2001–2004: blood sampling results for infections with W. bancrofti (Ghana)
Final analysis of the entomological data for 2005 is being compiled. Data for the first three years showed an overall decreasing trend in the annual transmission potential (ATP) (from 356.2 in 2001, through 296.6 in 2002, to 229.4 in 2003) (fig. 2). However, when this was broken down to the contributions made by different Anopheles species, it was realized that, while the ATP of An. funestus had significantly decreased, that for An. gambiae had not. A critical examination of the data indicated that the ATP is being influenced by collections from one site (Mampong); the current analysis will take this into account. The ATP is mirrored in the annual infective biting rate (fig. 3).
Annual transmission potential (ATP) trends for the main Anopheles vector species from 2001 to 2004 (Ghana)
Annual infective biting rate (AIBR) trends for the main Anopheles vector species from 2001 to 2004 (Ghana)
The treatment coverage based on total study population was 67% with 0.6% having side effects in 2002, and 69.4% with 0.4% having side effects in 2003.
Parasitological and clinical studies
Summary of the major remaining uncertainties and research questions, and suggestions for specific studies
The observation that Anopheles-transmitted W. bancrofti in the Bongo area of Ghana shows the process of limitation  indicates that the situation needs clarification in terms of the species involved in transmission. A similar study to look at specific Anopheles species is necessary.
The study on trends in transmission after MDA in the eight communities in Ghana indicates that some of the vectors (An. gambiae s.s.) are able to pick up the infection and transmit infective larvae at very low levels of microfilaraemia in humans. Although the 2004 entomological analysis is yet to be completed, it may be necessary to consider continuing the study for longer than the five years of MDA planned by the national programme. As now planned, the study will end after four years of MDA, but this may not be enough to arrive at a definite conclusion.
Pichon  postulated that low level prevalence and intensity of microfilaraemia may increase the mean lifespan of some of the local Anopheles species and may worsen the problem posed by malaria. How this increase in mean lifespan affects the transmission of W. bancrofti has not, however, been examined.
Issues to be addressed to increase the chances of eliminating lymphatic filariasis by mass drug administration
Suggestions for specific studies
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3. Bryan JH, McMahon P, Barnes A, (1990) Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 3. Uptake and damage to ingested microfilariae by Anopheles gambiae, An arabiensis, An. merus and An. funestus in East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 84: 265-268.
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18. Southgate BA, Bryan JH, (1992) Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 4. facilitation, limitation proportionality and their epidemiological significance. Transactions of the Royal Society of Tropical Medicine and Hygiene 86: 523-530.
20. Touré YT, (1979) Bio-écologie des anophèles (Diptera, culcidea) dans une zone rurale de savane soudanienne au Mali (village de Banambani). Incidence sur la transmission du paludisme et de la filariose de bancroft Mali, Bamako:Thèse de 3ème cycle, Centre Pédagogique Supérieur .
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