An apparent halt to the decline of Simulium woodi in the Usambara foci of onchocerciasis in Tanzania.

Abstract

There are currently 11–13 foci of human onchocerciasis recognised in Tanzania (Raybould and White, 1979; Maegga, 1991). The disease was first recorded in the country by Fischer (1932), from Rungwe (within the modern-day Tukuyu focus). Nine years later the disease was recorded by Gabathuler and Gabathuler (1947), from Ulanga district, in what is now known as the Mahenge focus. It was not until 1957 that a third focus was discovered in Tanzania, in the eastern block of the Usambara mountains (in Tanga region), by Mario Giaquinto-Mira (Woodman, 1958). Another focus was found in 1964, in the western block of the same mountains (Laing and Wegesa, 1965). Since 1963 the human onchocerciasis in the Usambara mountains has been the subject of research based at the East African Institute of Malaria and Vector-borne Diseases in Amani (now the Amani Medical Research Centre of the National Institute for Medical Research). Data collected in 1963–1964 indicated that, in several study sites in the Eastern Usambara focus, the mean prevalence of human infection with Onchocerca volvulus was 32% (Laing and Wegesa, 1965). When four localities in this focus were resurveyed in 1970, mean prevalence in the four sites was found to have increased to 46% (from the 29% recorded in 1963–1964), possibly because increasing agricultural activity had resulted in increased exposure to vector biting (Wegesa and Chimtawi, 1971). In 1984, however, Muro and Mziray (1990) resurveyed nine localities from the 1963–1964 survey and found that mean prevalence had decreased to 26% (from the 33% recorded in the same sites in 1963–1964), possibly because of continuing deforestation. Compared with its eastern counterpart, the Western Usambara focus is less well known, but Sprengel (1967, 1968) did much to define it (finding a mean prevalence, of human infection, of 37%) and Dunbar (1975) extended its known range. In the 1990s about 5000 and 19,000 people were thought to be infected with O. volvulus in the Western and Eastern Usambara foci, respectively (Mwaiko et al., 1990; Walsh and Maegga, 1996). In 2001 the National Onchocerciasis Control Programme of the Tanzanian Ministry of Health started annual, community-directed treatment with ivermectin (CDTI) simultaneously over all of the endemic areas in Tanga region (i.e. the Eastern Usambara mountains within the Muheza and Mchinga districts and the Western Usambara mountains within the Korogwe and Lushoto districts). The vector of O. volvulus throughout the Usambaras is Simulium woodi (a member of the S. neavei group) (Raybould and White, 1979). When Raybould (1967) studied transmission of the parasite, through weekly biting catches over 13 months (1963–1964) at a single site near Amani, in the Eastern Usambara focus, he found a mean daily biting rate (DBR) for S. woodi of 42·8, with 33·6% of the collected flies found parous and 17·3% of the parous flies found infected with O. volvulus. The corresponding mean DBR recorded in two catches at the same site in 1974–1975 was, however, only 5% of that recorded in 1963–1964 (Raybould, 1975), and Raybould (1975) reported that ‘periodic collections from other areas have shown that this [marked reduction in DBR] is not just a local phenomenon’. When they carried out vector collections from the same site near Amani over 12 months in 1985–1986, Muro and Raybould (1990) recorded a mean DBR for S. woodi of 5·64, with the percentage of the collected flies found parous ‘the same’ as seen in 1963–1964 but only 3·2% of the parous found infected. The falls seen in DBR since the 1960s were attributed by Muro and Raybould (1990) to deforestation, which had made the habitat unsuitable for S. woodi. Muro and Raybould (1990) postulated that the decline in S. woodi DBR may have come to an end at the time of their study because of then-recent programmes of re-afforestation. This suggestion appeared to be supported by Walsh and Maegga (1996), who visited Amani in November 1995 and reported that ‘the larvae and pupae of S. woodi were certainly common at traditional sites’. To investigate whether the population decline in S. woodi has been arrested or has continued, the Western and Eastern Usambara foci were visited in March 2010, when human biting catches were carried out by a single vector collector for 5 h (06·30–09·30 and 16·30–18·30 hours) at each of seven sites (see Table). Since Raybould (1967) described the diurnal biting cycle at Amani-Mfenesini for March, it was possible to assume that the eight flies caught at this site, over 5 h, represented about 71·5% of a full day’s catch (06·30–18·30 hours), and, from this, to estimate a corresponding DBR of 11·2. Although all 21 flies caught were identified as members of the S. neavei group (and were, therefore, probably S. woodi), they were not dissected to see if they were parous or infected with O. volvulus because sample sizes were too small to make such investigation meaningful. It is clear, however, that anthropophagy is continuing among the blackflies in both the Eastern and Western Usambara foci. It is also clear that the DBR recorded at Amani-Mfenesini in March 2010 (11·2; present study) was substantially lower than those recorded in March 1964 (with a mean of 57 and a range of 35–76 over 4 days; Raybould, 1967), markedly higher than the value (5% of the earlier value, or about 2·8) apparently recorded in March 1975 (Raybould, 1975) and similar to the value (12) recorded by Muro and Raybould (1990) in March 1986. When the DBR recorded at Amani-Mfenesini are plotted against the collection dates (see Figure), they appear to have dropped between 1964 and 1975 but subsequently remained fairly stable for approximately 35 years, up to the recent (2010) survey. Trends in daily biting rate (DBR) for the month of March, between 1964 and 2010, at Amani-Mfenesini. The values shown for 1975 and 2010 are estimates based on the limited data available. The numbers of blackflies caught on human bait in March 2010, over 5 h of collection at each site It is unclear whether the temporal trends seen in DBR (Fig.) have had any effect on the prevalence and intensity of onchocerciasis in the human populations living in the Usambara foci. Muro and Mziray (1990) reported a small drop in prevalence over a couple of decades, from 33% in 1963–1964 to 26% in 1984, which they attributed to lower vector populations. It is unclear whether S. woodi can maintain the transmission of O. volvulus when its DBR are as low as those recorded in the foci over the last three decades. It is possible that the stable transmission of O. volvulus is near its lower critical point in the Usambara foci and therefore might be very vulnerable to control efforts such as CDTI or vector control. In the Itwara focus in Uganda, S. neavei maintained transmission at DBR of around 20–60 (Garms et al., 2009). Probably because S. neavei is a highly anthropophilic and efficient vector, 4 years of ivermectin distribution in Itwara had little effect on transmission (Garms et al., 2009). As a consequence, a vector-elimination campaign was initiated and, since September 2003, S. neavei has never been seen in the focus (Garms et al., 2009). Members of the S. neavei group are often considered particularly vulnerable to vector elimination because of their limited flight range and restriction to well defined patches of forest (Garms et al., 2009). Raybould (1975) suggested the possibility of vector control in the Eastern Usambara focus, pointing out that, because of the long period of larval development of S. woodi near Amani (Raybould and Mhiddin, 1978), control operations would require no more than monthly application of insecticide. Garms et al. (2009) found that monthly treatments over approximately 18 months were sufficient to eliminate S. neavei from the various sub-foci in the Itwara focus. Although Walsh and Maegga (1996) considered that the limits of the Eastern Usambara focus needed to be better defined, they also thought that vector elimination was both feasible and desirable in the focus.