“Slash and Clear”, a Community-Based Vector Control Method to Reduce Onchocerciasis Transmission by Simulium sirbanum in Maridi, South Sudan: A Prospective Study

Onchocerciasis is a disease of major public health importance in Maridi County, South Sudan, where it is associated with a high prevalence of epilepsy, including nodding syndrome [1,2]. Half the adult volunteers tested for onchocerciasis in the Maridi villages were found to have Onchocerca volvulus microfilariae in their skin snips, while over 80% of persons with epilepsy (PWE) were also infected [3]. Communities living close to the Maridi dam more often complained of intense black fly nuisance and were more affected by seizure disorders. In 2018, in a door-to-door survey, an epilepsy prevalence of 4.4% and annual incidence of 373.9/100,000 person years were documented in villages close to the Maridi River, with the highest prevalence (11.9%) observed in Kazana 2, a village close to the Maridi dam [1]. For many years, mass drug administration of ivermectin had been interrupted in the area and only 40.8% of the population took ivermectin in 2017 [1].

Vector control using larvicides was the primary strategy of successful onchocerciasis control programs in West Africa which operated from 1974 to 2002 [4]. However, the implementation of larvicide treatments is labor-intensive, costly and potentially harmful to the environment. Moreover, insecticide resistance is a concern for the long-term success of this method. A study in multiple communities in northern Uganda using a “slash and clear” method resulted in an 89−99% decline in vector biting rates that lasted up to 120 days post-intervention [5]. We investigated the feasibility and efficacy of this “slash and clear” method in reducing black fly biting rates at the Maridi dam, the only black fly breeding site identified in the Maridi central area.

Simulium damnosum s.l. is the only known vector of onchocerciasis in South Sudan and occurs in most rapidly flowing rivers and streams [6], including the Maridi River (or River Gel) at the Maridi dam [7,8]. The precise cytospecies within the S. damnosum complex present at Maridi has never been described, although both S. damnosum s. str. and S. sirbanum have been identified from tributaries of the Bahr el Ghazal River, northwest of Maridi [8], and from rivers in northern Uganda (Post, unpublished data).

The chromosomal characterization of the larvae collected from the Maridi dam clearly indicates that S. sirbanum is the main (or only) vector species in the area. Furthermore, chromosomal characterization is consistent with the resident cytotype being the ‘Type IV form’ of S. sirbanum [19]. However, the small number of specimens examined cannot rule out the possibility of the ‘Sudanese form’ of S. sirbanum, but this is unlikely because the two males extracted from pupae were found to have ‘Type IV’ scutal patterns, which is characteristic of the ‘Type IV form’, whilst the ‘Sudanese form’ usually has type III scutal patterns [20].

Our study shows that black fly biting rates in Maridi, South Sudan, were drastically reduced by >90% in all sites following implementation of the “slash and clear” exercise, and biting rates remained low for several months afterwards. This finding is very much in agreement with that of Baker and Abdelnur [20], who cleared vegetation from a single site on the River Bussere about 25 km upstream of Wau, where S. sirbanum represented around 90% of all larvae identified [8]. They did not measure the effect on biting rates, but they reported that breeding was “virtually eliminated”. More recently, in northern Uganda, Jacob et al. [5] reported that removal of trailing vegetation from S. damnosum s. str. breeding sites resulted in a dramatic reduction in biting rates (ca. 90%). However, for the Maridi dam, the trend in biting rates was slightly different from Uganda because of a spike observed during the first month post-intervention. This was likely due to some remaining mature larvae and pupae that might have been missed from being scraped from the concrete dam spillway, and these later hatched and contributed to the population of flies recorded in February 2020. This has provided a unique lesson when undertaking this intervention in ecological areas where S. damnosum s.l. is also breeding on concrete and rocks, whereas in rivers, where breeding is entirely on trailing vegetation, once this is removed, no residual black fly population is observed. However, the slow population recovery in S. damnosum s.l. observed seven months post-intervention was most likely attributed to the slow re-growth of vegetation on the spillway at the Maridi dam (Figure 1, Panel C).

Vegetation provides support for attachment of young stages of the vector and directly impacts on the population at breeding sites, as was earlier reported also in Uganda [5]. The reduction in parity rate observed post-“slash and clear” intervention could be attributed to the success of this intervention, as the flies coming out are those newly hatched from the breeding sites. Lewis earlier reported that the percentage of nulliparous flies is expected to rise after heavy rains and when rivers have risen, and this is due to the emergence of fresh flies [17]. In the case of the sites at the Maridi dam, dissection for parity was performed towards the end of the rainy season, and the variation in parity rate pre- and post-intervention may require a prolonged study.

In Maridi, the “slash and clear” technique was rapidly accepted by the local population. Community volunteers were trained during the initial “slash and clear” intervention and were able to repeat the intervention satisfactorily with limited supervision the second time. Given the past nuisance caused by black flies in these villages and the high incidence of onchocerciasis-associated epilepsy, the community is highly motivated to continue this intervention in the coming years. To further decrease black fly biting rates, the plan is to repeat the “slash and clear” intervention in the future every seven months.

A limitation of our study is that black fly infectivity rates could not be determined. Black flies were collected to be pool-screened with O. volvulus PCR, but because they had not been adequately preserved, this screening could not be performed.

Vector control is currently underutilized in onchocerciasis control programs in Africa due to inadequate resources for costly larviciding and lack of adequate entomological workforces [21], thus the need for research into other simpler vector control approaches.

The recent innovation of “slash and clear” has provided an additional tool for control and elimination of onchocerciasis, and is advocated as an alternative strategy [13]. A recent modeling study showed that supplementing annual drug treatments with “slash and clear”, even if vegetation is cleared only once per year, can significantly accelerate the achievement of onchocerciasis elimination [14]. However, the feasibility and efficacy of the “slash and clear” method may depend on local vegetation and other riverine features. The Maridi dam was an excellent site for implementing this method because it was the only productive site of S. damnosum s.l. breeding, and in addition, is the main source of drinking water for Maridi town and the villages close to it, therefore raising concerns from communities about the application of larvicides. This environmentally friendly intervention is simple and inexpensive to perform, requiring equipment commonly found in rural communities in Africa [4]. However, further field studies should be carried out in other geographical settings in the African region with other vector cytospecies. A cluster randomized trial to determine the effectiveness of the “slash and clear” intervention on O. volvulus transmission is currently ongoing in Cameroon [22], along with further work in northern Uganda [23].

The high baseline biting rates observed at the Maridi dam were not surprising; indeed, dam spillways have been reported to be excellent black fly breeding sites in the past [24,25,26,27,28]. Such areas need to be prioritized for onchocerciasis elimination efforts, since ivermectin alone may not be sufficient to achieve elimination in the face of such productive breeding sites, and additional tools may be needed. A combination of both CDTI and community-directed removal of black fly larval attachment sites is therefore recommended in these settings.

A weakness of the study is that the dam spillway was the only black fly breeding site in the area. Therefore, it was not possible to include a control site that was untreated to adjust for overall variations in black fly numbers caused by climatic changes. Dam spillways are an artificial environment where the degree of breeding is closely associated with the amount of water flowing over the dam. However, no data about water flow were available at the Maridi dam. Since the insecurity in the area in 2013, the qualified staff at the dam have left. Since then, there have been no regular measurements of water levels at the dam reservoir, and the water gates of the dam were poorly managed to release water when there is water overspill. Therefore, the overspill of water through the dam spillway is continuous throughout the year, with higher levels in the rainy season (March to November) and minimal levels during the dry season (December to February). However, without the “slash and clear”, the vegetation growth is present throughout the year.

The “slash and clear” method was found to be a very effective, simple, and cheap community-based method to reduce biting rates caused by S. sirbanum from a local breeding site. When repeated at least annually together with high coverage of community-directed treatment with ivermectin, it has the potential to considerably accelerate onchocerciasis elimination.