Are herders protected by their herds? An experimental analysis of zooprophylaxis against the malaria vector Anopheles arabiensis

Background The number of Anopheles arabiensis (Diptera: Culicidae) and Anopheles pharoensis caught by human and cattle baits was investigated experimentally in the Arba Minch district of southern Ethiopia to determine if attraction to humans, indoors or outdoors, was affected by the presence or absence of cattle. Methods Field studies were made of the effect of a surrounding ring (10 m radius) of 20 cattle on the numbers of mosquitoes collected by human-baited sampling methods (i) inside or (ii) outside a hut. Results The numbers of An. arabiensis caught outdoors by a human landing catch (HLC) with or without a ring of cattle were not significantly different (2 × 2 Latin square comparisons: means = 24.8 and 37.2 mosquitoes/night, respectively; n = 12, P > 0.22, Tukey HSD), whereas, the numbers of An. pharoensis caught were significantly reduced (44%) by a ring of cattle (4.9 vs. 8.7; n = 12, P 0.999) or An. pharoensis (n = 48, P > 0.870). The HLC catches indoors vs. outdoors were not significantly different for either An. arabiensis or An. pharoensis (n = 12, P > 0.969), but for An. arabiensis only, the indoor catch was reduced significantly by 49% when the hut was surrounded by cattle (Tukey HSD, n = 12, P > 0.01). Conclusions Outdoors, a preponderance of cattle (20:1, cattle:humans) does not provide any material zooprophylactic effect against biting by An. arabiensis. For a human indoors, the presence of cattle outdoors nearly halved the catch. Unfortunately, this level of reduction would not have an appreciable impact on malaria incidence in an area with typically > 1 infective bite/person/night. For An. pharoensis, cattle significantly reduced the human catch indoors and outdoors, but still only by about half. These results suggest that even for traditional pastoralist communities of East Africa, the presence of large numbers of cattle does not confer effective zooprophylaxis against malaria transmitted by An. arabiensis or An. pharoensis

Onchocerciasis transmission in Ghana: biting and parous rates of host-seeking sibling species of the Simulium damnosum complex

Background: Ghana is renowned for its sibling species diversity of the Simulium damnosum complex, vectors of Onchocerca volvulus. Detailed entomological knowledge becomes a priority as onchocerciasis control policy has shifted from morbidity reduction to elimination of infection. To date, understanding of transmission dynamics of O. volvulus has been mainly based on S. damnosum sensu stricto (s.s.) data. We aim to elucidate bionomic features of vector species of importance for onchocerciasis elimination efforts. Methods: We collected S. damnosum sensu lato from seven villages in four Ghanaian regions between 2009 and 2011, using standard vector collection, and human- and cattle-baited tents. Taxa were identified using morphological and molecular techniques. Monthly biting rates (MBR), parous rates and monthly parous biting rates (MPBR) are reported by locality, season, trapping method and hour of collection for each species. Results: S. damnosum s.s./S. sirbanum were collected at Asubende and Agborlekame, both savannah villages. A range of species was caught in the Volta region (forest-savannah mosaic) and Gyankobaa (forest), with S. squamosum or S. sanctipauli being the predominant species, respectively. In Bosomase (southern forest region) only S. sanctipauli was collected in the 2009 wet season, but in the 2010 dry season S. yahense was also caught. MBRs ranged from 714 bites/person/month at Agborlekame (100% S. damnosum s.s./S. sirbanum) to 8,586 bites/person/month at Pillar 83/Djodji (98.5% S. squamosum). MBRs were higher in the wet season. In contrast, parous rates were higher in the dry season (41.8% vs. 18.4%), resulting in higher MPBRs in the dry season. Daily host-seeking activity of S. damnosum s.s./S. sirbanum was bimodal, whilst S. squamosum and S. sanctipauli had unimodal afternoon peaks. Conclusions: The bionomic differences between sibling species of the S. damnosum complex need to be taken into account when designing entomological monitoring protocols for interventions and parameterising mathematical models for onchocerciasis control and elimination

Onchocerciasis transmission in Ghana: Persistence under different control strategies and the role of the simuliid vectors

Background: The World Health Organization (WHO) aims at eliminating onchocerciasis by 2020 in selected African countries. Current control focuses on community-directed treatment with ivermectin (CDTI). In Ghana, persistent transmission has been reported despite long-term control. We present spatial and temporal patterns of onchocerciasis transmission in relation to ivermectin treatment history. Methodology/Principal Findings: Host-seeking and ovipositing blackflies were collected from seven villages in four regions of Ghana with 3–24 years of CDTI at the time of sampling. A total of 16,443 flies was analysed for infection; 5,812 (35.3%) were dissected for parity (26.9% parous). Heads and thoraces of 12,196 flies were dissected for Onchocerca spp. and DNA from 11,122 abdomens was amplified using Onchocerca primers. A total of 463 larvae (0.03 larvae/fly) from 97 (0.6%) infected and 62 (0.4%) infective flies was recorded; 258 abdomens (2.3%) were positive for Onchocerca DNA. Infections (all were O. volvulus) were more likely to be detected in ovipositing flies. Transmission occurred, mostly in the wet season, at Gyankobaa and Bosomase, with transmission potentials of, respectively, 86 and 422 L3/person/month after 3 and 6 years of CDTI. The numbers of L3/1,000 parous flies at these villages were over 100times the WHO threshold of one L3/1,000 for transmission control. Vector species influenced transmission parameters. At Asubende, the number of L3/1,000 ovipositing flies (1.4, 95% CI = 0–4) also just exceeded the threshold despite extensive vector control and 24 years of ivermectin distribution, but there were no infective larvae in host-seeking flies. Conclusions/Significance: Despite repeated ivermectin treatment, evidence of O. volvulus transmission was documented in all seven villages and above the WHO threshold in two. Vector species influences transmission through biting and parous rates and vector competence, and should be included in transmission models. Oviposition traps could augment vector collector methods for monitoring and surveillance

Onchocerciasis transmission by the Bioko form of Simulium yahense Vajime & Dunbar 1975 (Diptera: Simuliidae)

The vectorial abilities of the endemic form of Simlium yahense VAJLME & DUNBAR,1975 that occurs on the island of Bioko, Equatorial Guinea, were investigated in relation to ivermectin treatments. Although ivermectin has been administered in Bioko since 1990, coverage remains low with about half the island's population treated. There were no data on levels of parasitism with Onchocerca volvulus in Simulium yahense collected prior to the treatments, although one data-set from a site at Sampaca is based on flies collected in 1993. These data on transmission rates were compared with more recent ones at Sampaca, which did not show any evidence of a decrease. Data from two other sites (Balacha de Riaba and Musola) collected during the African Programme for Onchocerciasis Control (APOC) project in 1999-2001 did not show any evidence of declines in transmission rates either, but three of four transmission indices measured at Barleycorn did decrease. Transmission rates (ATPs of398-2161) and levels of parasitism in the flies (means of7.7 LlIL2 per fly with LIIL2 and 4.4 L3 in the head per fly with L3 in the head) were typical for the West African forest zon

Methods used to obtain host-independent (A, B) and host-dependent (C, D) adult female blackfly samples.

<p><b>(A)</b> Bellec (sticky) trap situated above rapids; <b>(B)</b> Monk’s Wood (light) trap placed near presumed breeding sites; <b>(C)</b> human-baited tent; <b>(D)</b> cow-baited tent. <b>A</b> and <b>B</b> illustrate traps to collect ovipositing flies; <b>C</b> and <b>D</b> depict methods to obtain host-seeking flies.</p

Maps showing the location of Ghana (A), the boundaries and start dates for the Onchocerciasis Control Programme (OCP) phases (B), and the seven Ghanaian study sites (C).

<p>The OCP began vector control operations across West Africa in 1975. Asubende received vector control from 1986, which was interrupted several times during 1987–1989 because of community trials of the impact of ivermectin mass treatment on transmission and microfilarial loads. At the time of closure of the OCP in 2002, the Asubende focus was incorporated into a special intervention zone (SIZ) due to on-going transmission. The breeding sites at Asukawkaw Ferry, Dodi Papase and Pillar 83 were first treated with larviciding insecticides during OCP experimental campaigns (reinvasion studies) in 1981 (see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003688#pntd.0003688.g002" target="_blank">Fig 2</a> of Cheke & Garms 1983 [<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003688#pntd.0003688.ref094" target="_blank">94</a>]), before becoming part of the South-eastern extension, which reached these river basins when it became fully operational in February 1988.</p

Therapeutic coverage of ivermectin treatment in all study villages.

<p>The plots show the percentage of the overall population treated at each ivermectin round since mass ivermectin distribution began: <b>(A)</b> Asubende and <b>(B)</b> Agborlekame in the Brong-Ahafo Region; <b>(C)</b> Asukawkaw Ferry, <b>(D)</b> Dodi Papase and <b>(E)</b> Pillar 83 in the Volta Region; <b>(F)</b> Bosomase in the Western Region, and <b>(G)</b> Gyankobaa in the Ashanti Region. The dashed lines are the best fit least squares polynomial functions to the data, presented to facilitate visual inspection of the coverage trends. Biannual ivermectin distribution started in 2009 in Asubende, Agborlekame and Gyankobaa, whilst annual distribution has continued in the remaining villages.</p

Proportions of infected and infective flies by season and sampling method for Bosomase and Gyankobaa.

<p>Data and error bars are as in Fig 3, but excluding the 2006 Bellec-caught flies collected at Bosomase, as during the pilot study comparisons with other fly collection methods were not conducted.</p

Vector control and ivermectin treatment history, current strategy and infection levels per village.

<p>^<b>a</b> CMFL = community microfilarial load as defined in [<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003688#pntd.0003688.ref019" target="_blank">19</a>], expressed as microfilariae (mf) per skin snip (ss)</p><p>^<b>b</b> CDTI = community-directed treatment with ivermectin</p><p>^<b>c</b> Flies infected with any <i>O</i>. <i>volvulus</i> larval stage</p><p>^<b>d</b> Flies infected with <i>O</i>. <i>volvulus</i> L3 larvae in heads and thoraces (the percentages of infected and infective flies were calculated from all flies, collected by both oviposition and host-seeking methods. Details of the total numbers dissected for each collection technique per village per season are presented in <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003688#pntd.0003688.s002" target="_blank">S2 Table</a>)</p><p>^<b>e</b> pre-treatment baseline prevalence unknown, with 2000 the earliest date available; multiple ivermectin treatments from 1993 to 1997. In 1992, a mapping survey of the Onchocerciasis Control Programme in West Africa extension stated that ‘the site of Djodji presents the highest transmission potentials of the Eastern extension’[<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003688#pntd.0003688.ref095" target="_blank">95</a>].</p><p>Vector control and ivermectin treatment history, current strategy and infection levels per village.</p

Proportions of infected and infective flies (assessed by heads and thoraces dissection) in study villages and years of ivermectin treatment.

<p>Infected flies (green bars) are those with any larval stage of <i>Onchocerca volvulus</i>; infective flies (blue bars) are those harbouring L3 larvae in heads and/or thoraces. Error bars are exact 95% confidence intervals. The results for Bosomase include the Bellec-caught flies obtained during the pilot study conducted at Bosomase in January–February 2006.</p