Research Article: Onchocerciasis Transmission in Ghana: Persistence under Different Control Strategies and the Role of the Simuliid Vectors

Date Published: April 21, 2015

Publisher: Public Library of Science

Author(s): Poppy H. L. Lamberton, Robert A. Cheke, Peter Winskill, Iñaki Tirados, Martin Walker, Mike Y. Osei-Atweneboana, Nana-Kwadwo Biritwum, Anthony Tetteh-Kumah, Daniel A. Boakye, Michael D. Wilson, Rory J. Post, María-Gloria Basañez, Charles Brockhouse.

Abstract: BackgroundThe 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 FindingsHost-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 100 times 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/SignificanceDespite 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.

Partial Text: The London Declaration on Neglected Tropical Diseases (NTDs) [1] and the World Health Organization’s (WHO) road map to accelerate progress for overcoming the impact of NTDs [2] have set goals for the elimination of human onchocerciasis by 2020 in selected African countries. Based on the results of epidemiological studies conducted in some foci of Mali, Senegal and Nigeria [3,4,5], it has been suggested that 14–17 years of annual (or biannual) ivermectin treatment may lead to local elimination of the infection reservoir in the absence of vector control. The repeatability of these achievements depends, in part, on the initial level of onchocerciasis endemicity, geographical and therapeutic coverage, treatment compliance and frequency, parasite susceptibility to ivermectin, and the intensity and seasonality of transmission, including the species composition of the simuliid vectors [6].

A total of 17,300 S. damnosum s.l. flies was collected, of which 6,142 (35.5%) were caught by vector collectors; 2,207 (12.8%) were trapped in the human-baited tents; 1,567 (9.1%) in the cow-baited tents; 7,212 (41.7%) on Bellec traps—including 3,352 (46.5% of the Bellec total) from the pilot study in Bosomase during the dry season in 2006—and 172 (1%) in Monk’s Wood light traps. A total of 16,478 (95.2%) blackflies was morphologically identified, of which 5,812 (35.3%) were dissected for parity in the field, with 4,247 (73.1%) nullipars and 1,565 (26.9%) parous flies. These nullipars were not further dissected for Onchocerca infection, but pooled samples of the nullipars were used as molecular controls, with no positive Onchocerca results obtained. The heads and thoraces of 12,196 flies (6,918 ovipositing flies, 3,713 host-seeking flies of unknown parity status and 1,565 known parous flies) were stained and dissected for Onchocerca spp. larvae. These, plus the known uninfected nullipars (4,247), totalled 16,443 flies whose infection status was assessed. A total of 97 (0.6%) was infected (with any larval stage) of which 58 (0.4%) were infective (with L3s in head and/or thorax), with 45 flies (0.3%) harbouring L3s in the head (S2 Table).

As the goals of onchocerciasis control programmes shift from morbidity reduction towards elimination, knowledge of ongoing transmission by local vector species is urgently required [8,9,10]. This enables entomological monitoring of programmes’ progress, and helps to understand the determinants of persistent transmission despite prolonged control interventions. We report O. volvulus transmission, in Ghanaian communities with different treatment and control histories, and its variation according to simuliid species composition, vector trapping technique and season.



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