Jean-Baptiste Rayaisse

Standardizing visual control devices for tsetse flies: West African species Glossina tachinoides, G. palpalis gambiensis and G. morsitans submorsitans.

Here we describe field trials designed to standardize tools for the control of Glossina tachinoides, G. palpalis gambiensis and G.morsitans submorsitans in West Africa based on existing trap/target/bait technology. Blue and black biconical and monoconical traps and 1 m2 targets were made in either phthalogen blue cotton, phthalogen blue cotton/polyester or turquoise blue polyester/viscose (all with a peak reflectance between 450–480 nm) and a black polyester. Because targets were covered in adhesive film, they proved to be significantly better trapping devices than either of the two trap types for all three species (up to 14 times more for G. tachinoides, 10 times more for G. palpalis gambiensis, and 6.5 times for G. morsitans submorsitans). The relative performance of the devices in the three blue cloths tested was the same when unbaited or baited with a mixture of phenols, 1-octen-3-ol and acetone. Since insecticide-impregnated devices act via contact with flies, we enumerated which device (traps or targets) served as the best object for flies to land on by also covering the cloth parts of traps with adhesive film. Despite the fact that the biconical trap proved to be the best landing device for the three species, the difference over the target (20–30%) was not significant. This experiment also allowed an estimation of trap efficiency, i.e. the proportion of flies landing on a trap that are caught in its cage. A low overall efficiency of the biconical or monoconical traps of between 11–24% was recorded for all three species. These results show that targets can be used as practical devices for population suppression of the three species studied. Biconical traps can be used for population monitoring, but a correction factor of 5–10 fold needs to be applied to captures to compensate for the poor trapping efficiency of this device for the three species.

Reducing Human-Tsetse Contact Significantly Enhances the Efficacy of Sleeping Sickness Active Screening Campaigns: A Promising Result in the Context of Elimination.

Background Control of gambiense sleeping sickness, a neglected tropical disease targeted for elimination by 2020, relies mainly on mass screening of populations at risk and treatment of cases. This strategy is however challenged by the existence of undetected reservoirs of parasites that contribute to the maintenance of transmission. In this study, performed in the Boffa disease focus of Guinea, we evaluated the value of adding vector control to medical surveys and measured its impact on disease burden. Methods The focus was divided into two parts (screen and treat in the western part; screen and treat plus vector control in the eastern part) separated by the Rio Pongo river. Population census and baseline entomological data were collected from the entire focus at the beginning of the study and insecticide impregnated targets were deployed on the eastern bank only. Medical surveys were performed in both areas in 2012 and 2013. Findings In the vector control area, there was an 80% decrease in tsetse density, resulting in a significant decrease of human tsetse contacts, and a decrease of disease prevalence (from 0.3% to 0.1%; p=0.01), and an almost nil incidence of new infections (<0.1%). In contrast, incidence was 10 times higher in the area without vector control (>1%, p<0.0001) with a disease prevalence increasing slightly (from 0.5 to 0.7%, p=0.34). Interpretation Combining medical and vector control was decisive in reducing T. b. gambiense transmission and in speeding up progress towards elimination. Similar strategies could be applied in other foci.

Epidemiology of sleeping sickness in Boffa (Guinea): where are the trypanosomes?

Human African Trypanosomiasis (HAT) in West Africa is a lethal, neglected disease caused by Trypanosoma brucei gambiense transmitted by the tsetse Glossina palpalis gambiensis. Although the littoral part of Guinea with its typical mangrove habitat is the most prevalent area in West Africa, very few data are available on the epidemiology of the disease in such biotopes. As part of a HAT elimination project in Guinea, we carried a cross-sectional study of the distribution and abundance of people, livestock, tsetse and trypanosomes in the focus of Boffa. An exhaustive census of the human population was done, together with spatial mapping of the area. Entomological data were collected, a human medical survey was organized together with a survey in domestic animals. In total, 45 HAT cases were detected out of 14445 people who attended the survey, these latter representing 50.9% of the total population. Potential additional carriers of T. b. gambiense were also identified by the trypanolysis test (14 human subjects and two domestic animals). No trypanosome pathogenic to animals were found, neither in the 874 tsetse dissected nor in the 300 domestic animals sampled. High densities of tsetse were found in places frequented by humans, such as pirogue jetties, narrow mangrove channels and watering points. The prevalence of T. b. gambiense in humans, combined to low attendance of the population at risk to medical surveys, and to an additional proportion of human and animal carriers of T. b. gambiense who are not treated, highlights the limits of strategies targeting HAT patients only. In order to stop T. b. gambiense transmission, vector control should be added to the current strategy of case detection and treatment. Such an integrated strategy will combine medical surveillance to find and treat cases, and vector control activities to protect people from the infective bites of tsetse.

Updating the Northern Tsetse Limit in Burkina Faso (1949–2009): Impact of Global Change

The northern distribution limit of tsetse flies was updated in Burkina Faso and compared to previous limits to revise the existing map of these vectors of African trypanosomiases dating from several decades ago. From 1949 to 2009, a 25- to 150-km shift has appeared toward the south. Tsetse are now discontinuously distributed in Burkina Faso with a western and an eastern tsetse belt. This range shift can be explained by a combination of decreased rainfall and increased human density. Within a context of international control, this study provides a better understanding of the factors influencing the distribution of tsetse flies.

Explaining the Host-Finding Behavior of Blood-Sucking Insects: Computerized Simulation of the Effects of Habitat Geometry on Tsetse Fly Movement

Background Male and female tsetse flies feed exclusively on vertebrate blood. While doing so they can transmit the diseases of sleeping sickness in humans and nagana in domestic stock. Knowledge of the host-orientated behavior of tsetse is important in designing bait methods of sampling and controlling the flies, and in understanding the epidemiology of the diseases. For this we must explain several puzzling distinctions in the behavior of the different sexes and species of tsetse. For example, why is it that the species occupying savannahs, unlike those of riverine habitats, appear strongly responsive to odor, rely mainly on large hosts, are repelled by humans, and are often shy of alighting on baits? Methodology/Principal Findings A deterministic model that simulated fly mobility and host-finding success suggested that the behavioral distinctions between riverine, savannah and forest tsetse are due largely to habitat size and shape, and the extent to which dense bushes limit occupiable space within the habitats. These factors seemed effective primarily because they affect the daily displacement of tsetse, reducing it by up to ∼70%. Sex differences in behavior are explicable by females being larger and more mobile than males. Conclusion/Significance Habitat geometry and fly size provide a framework that can unify much of the behavior of all sexes and species of tsetse everywhere. The general expectation is that relatively immobile insects in restricted habitats tend to be less responsive to host odors and more catholic in their diet. This has profound implications for the optimization of bait technology for tsetse, mosquitoes, black flies and tabanids, and for the epidemiology of the diseases they transmit.

Tsetse Control and the Elimination of Gambian Sleeping Sickness

Sleeping sickness, or Human African Trypanosomiasis (HAT), is caused by two distinct parasites. In East and Southern Africa, Trypanosoma brucei rhodesiense causes the Rhodesian form of the disease (about 2% of all reported cases [1]). In Central and West Africa, T. b. gambiense causes the Gambian form of the disease (G-HAT—about 98% of all reported cases [1]). The disease normally affects remote rural communities. The people most at risk are those working outdoors for long periods, as they are most exposed to the bite of the tsetse fly (Glossina spp.: Diptera), which transmits the parasites. The comparable diseases which occur in livestock, collectively termed African Animal Trypanosomiasis (AAT), are a significant brake on African development [2]. Among the 31 tsetse species, the most important vectors of G-HAT are Glossina fuscipes and Glossina palpalis, which are riverine tsetse species (Palpalis group). Since the start of the 20th century, HAT has occurred in three huge epidemics. The most recent was in the 1990s when the annual cases officially reported to WHO peaked at 37,385 in 1998. It is widely acknowledged this severely underestimated actual numbers infected, which may have been as high as 450,000 in 1999 [3]. Untreated disease is normally fatal, so undoubtedly, many people infected in these epidemics died as a result. Although treatments for the disease have improved [4], they are still complex and difficult to administer particularly in the resource-poor settings where the disease thrives. There is no vaccine or chemoprophylaxis to prevent HAT and little prospect of either being developed in the near future. Vector control therefore remains the only means of protecting people from infection. Rhodesian HAT (R-HAT) is a zoonosis. As a consequence, vector control plays a key part in its control, and medical interventions are only used for humanitarian purposes. In contrast, G-HAT is generally considered to be an anthroponosis, and control has relied heavily on active and/or passive case detection and treatment programmes [5]. However, modelling [6], historical investigations [7], and practical interventions [8,9] have clearly demonstrated the role that vector control can play in control of G-HAT, but it was considered too expensive and difficult to deploy in the resource poor settings of HAT foci. In consequence, a study was started in 2006 to try to find a simpler and cheaper alternative for vector control suitable for G-HAT foci. The original hypothesis was that modifying insecticide-treated targets was the most likely means of producing a more cost-efficient vector control method for use in G-HAT foci. Two separate approaches were tried—to develop odours for use with targets or to change the visual characteristics of the target. The crucial finding was that a tiny target consisting of a small square of blue cloth flanked by a similar sized piece of black netting (Fig 1) was highly effective and would be about ten times more cost-effective than traps or large targets in control campaigns for the Palpalis (riverine) group tsetse flies responsible for the transmission of the vast majority of HAT [10–12]. This is in very strong contrast to Morsitans (savanna) group tsetse flies, which require much larger targets (1–2 m2). Importantly, it was found that all of the major G-HAT vectors responded well to tiny targets [13]. In addition, vegetation growth around tiny targets is a much smaller problem [14] than is the case for the large targets used against Morsitans group flies. In contrast to Morsitans group flies, odours seem to play only a minor role in the attraction of Palpalis group flies [15,16]. A modelling approach suggests that habitat geometry is the reason why Palpalis group flies are more dependent on sight than odour [17]. The general expectation is that relatively immobile insects in restricted habitats are more dependent on a thorough, vision-based search of their environment and that they are more wide-ranging in their diet. Fig 1 A tiny target in a typical setting in Uganda. Inevitably, the targets are gradually degraded by challenges in the environment, and the worst problems are floods, fallen targets, and the 6-month effective life of the insecticide in the tiny target [18]. As a consequence, current practice has been to deploy tiny targets once or twice per year, and the method has been successful in practice [9,18]. The aim in HAT foci is not to eradicate tsetse (although eradication should be embraced if feasible), but to stop transmission by reducing tsetse—human contact, and modelling suggests that this does not require complete removal of tsetse flies [6]. In addition, the reported time course of disease in humans is typically 3–4 years so that a fixed period of interrupted transmission may be sufficient to eliminate HAT in a focus. This approach is basically similar to the successful World Bank-funded OCP programme, which has led to the elimination of onchocerciasis as a public health problem in West Africa [19]. The approach had also been applied successfully in HAT foci of Ivory Coast in the 1980s and 1990s by Laveissiere and colleagues [8], although at that time the control techniques used were not considered to be sustainable and cost effective. Consequently, to test the utility of tiny targets, studies were started in G-HAT foci (typically 500–3,000 km2). To re-emphasise, the goal is to reduce tsetse numbers below a threshold for transmission for a defined period to either eliminate or reduce transmission in a HAT focus, thereby giving screen-and-treat programmes a far greater chance of success [20]. For example, a previously published model [6] has been used along with figures from West Nile, Uganda to calculate the impact of various levels of vector control on transmission in that region (Fig 2) [18]. In practice, the level of control actually achieved in that region was >90%, which exceeds the levels required to interrupt transmission (Fig 2) [18]. How long control must continue is a researchable question but, given the time course of the disease in humans, it is likely to be several years. Presumably, it is also dependent on the distribution of the parasite in the human population and/or the existence of reservoir hosts. Current discussions have been focusing on 4–5 years of control. Fig 2 To obtain an estimate of the level of tsetse control required to stop transmission, a published model was rearranged [6].

Quality of sterile male tsetse after long distance transport as chilled, irradiated pupae

Background Tsetse flies transmit trypanosomes that cause human and African animal trypanosomosis, a debilitating disease of humans (sleeping sickness) and livestock (nagana). An area-wide integrated pest management campaign against Glossina palpalis gambiensis has been implemented in Senegal since 2010 that includes a sterile insect technique (SIT) component. The SIT can only be successful when the sterile males that are destined for release have a flight ability, survival and competitiveness that are as close as possible to that of their wild male counterparts. Methodology/Principal Findings Tests were developed to assess the quality of G. p. gambiensis males that emerged from pupae that were produced and irradiated in Burkina Faso and Slovakia (irradiation done in Seibersdorf, Austria) and transported weekly under chilled conditions to Dakar, Senegal. For each consignment a sample of 50 pupae was used for a quality control test (QC group). To assess flight ability, the pupae were put in a cylinder filtering emerged flies that were able to escape the cylinder. The survival of these flyers was thereafter monitored under stress conditions (without feeding). Remaining pupae were emerged and released in the target area of the eradication programme (RF group). The following parameter values were obtained for the QC flies: average emergence rate more than 69%, median survival of 6 days, and average flight ability of more than 35%. The quality protocol was a good proxy of fly quality, explaining a large part of the variances of the examined parameters. Conclusions/Significance The quality protocol described here will allow the accurate monitoring of the quality of shipped sterile male tsetse used in operational eradication programmes in the framework of the Pan-African Tsetse and Trypanosomosis Eradication Campaign.

Detection and identification of pathogenic trypanosome species in tsetse flies along the Comoé River in Côte d’Ivoire

In order to identify pathogenic trypanosomes responsible for African trypanosomiasis, and to better understand tsetse-trypanosome relationships, surveys were undertaken in three sites located in different eco-climatic areas in Côte d’Ivoire during the dry and rainy seasons. Tsetse flies were caught during five consecutive days using biconical traps, dissected and microscopically examined looking for trypanosome infection. Samples from infected flies were tested by PCR using specific primers for Trypanosoma brucei s.l., T. congolense savannah type, T. congolense forest type and T. vivax. Of 1941 tsetse flies caught including four species, i.e. Glossina palpalis palpalis, G. p. gambiensis, G. tachinoides and G. medicorum, 513 (26%) were dissected and 60 (12%) were found positive by microscopy. Up to 41% of the infections were due to T. congolense savannah type, 30% to T. vivax, 20% to T. congolense forest type and 9% due to T. brucei s.l. All four trypanosome species and subgroups were identified from G. tachinoides and G. p. palpalis, while only two were isolated from G. p. gambiensis (T. brucei s.l., T. congolense savannah type) and G. medicorum (T. congolense forest, savannah types). Mixed infections were found in 25% of cases and all involved T. congolense savannah type with another trypanosome species. The simultaneous occurrence of T. brucei s.l., and tsetse from the palpalis group may suggest that human trypanosomiasis can still be a constraint in these localities, while high rates of T. congolense and T. vivax in the area suggest a potential risk of animal trypanosomiasis in livestock along the Comoé River.

Genetic correlations within and between isolated tsetse populations: what can we learn?

Isolated tsetse populations constitute a target for tsetse control programmes in endemic countries, since their isolation, if demonstrated, allows control without reinvasion risk from neighbouring populations. Population genetic parameters, such as the fixation index, have proven useful to assess isolation status, and should also give important information on the divergence time since isolation. We gathered results obtained from different datasets regarding several examples of putatively totally isolated tsetse populations of different tsetse species: Glossina palpalis gambiensis in Guinea, in the Niayes of Senegal, and in the sacred wood of Bama in Burkina Faso; G. tachinoides from Bitou and Pama in South-East Burkina Faso. The different levels of isolation were compared to differentiation between the two subspecies G. p. gambiensis and G. p. palpalis which both occur allopatrically along the Comoe River in Ivory Coast. We also use some historical evidence to calibrate differentiation speed and give estimates of time since separation for the different cases studied. Discrepancies mostly come from underestimate of effective population sizes, and we propose improving sampling design and genetic markers quality to circumvent such caveats.

Interactions comportementales et rythmes d’activité de Glossina palpalis gambiensis et G. tachinoides (Diptera : Glossinidae) en galerie forestière au Burkina Faso

Glossina palpalis gambiensis et G. tachinoides sont des vecteurs majeurs des trypanosomoses humaines et animales en Afrique de l’Ouest. Sur une partie de leur aire de répartition, elles sont présentes en sympatrie, mais très peu d’informations sont disponibles sur leurs interactions. Nous avons capturé ces deux espèces en utilisant un système attractif composé d’écrans de tissu noir/bleu/ noir muni de film adhésif, afin de retenir toutes les glossines posées et de pouvoir mesurer la hauteur à laquelle elles se sont posées, ainsi que leur rythme d’activité en fonction de l’heure de la journée. L’étude a eu lieu dans deux zones du sud du Burkina Faso : Kartasso en amont du fleuve Mouhoun, où seule G. p. gambiensis est présente, et Folonzo sur le fleuve Comoé, où les deux espèces cohabitent. Les résultats, sur 3 800 glossines capturées, montrent une forte prédominance des captures de G. tachinoides par rapport à G. p. gambiensis à Folonzo (84 % contre 16 % des captures respectivement). À Kartasso, où elle est seule, G. p. gambiensis est capturée en moyenne à 46 cm du sol. À Folonzo, G. p. gambiensis est en moyenne attrapée à une hauteur de 65 cm, et G. tachinoides à 55 cm, ces différences de hauteurs étant significatives. Les femelles sont capturées en général plus haut que les mâles. Les deux espèces montrent un rythme d’activité similaire en fonction de l’heure de capture, mais seule G. p. gambiensis réduit sa hauteur de vol aux heures les plus chaudes. Plusieurs hypothèses, non exclusives, sont évoquées pour expliquer ces hauteurs de capture différentes : la nature de la galerie forestière, un comportement d’approche qui différerait entre espèces, mais aussi la possibilité de phénomènes de compétition interspécifique en relation avec l’utilisation de ressources énergétiques limitées (métabolisme lié à la proline). Sont également discutées les conséquences possibles de ces différences de comportement sur les méthodes de lutte, par exemple lors de l’utilisation d’attractifs olfactifs qui pourraient avoir des efficacités distinctes en fonction de la hauteur de vol.