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      Ongoing Transmission of Onchocerca volvulus after 25 Years of Annual Ivermectin Mass Treatments in the Vina du Nord River Valley, in North Cameroon

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Background

          Recent reports of transmission interruption of Onchocerca volvulus, the causing agent of river blindness, in former endemic foci in the Americas, and more recently in West and East Africa, raise the question whether elimination of this debilitating disease is underway after long-term treatment of the population at risk with ivermectin. The situation in Central Africa has not yet been clearly assessed.

          Methods and findings

          Entomologic data from two former endemic river basins in North Cameroon were generated over a period of 43 and 48 months to follow-up transmission levels in areas under prolonged ivermectin control. Moreover, epidemiologic parameters of animal-borne Onchocerca spp. transmitted by the same local black fly vectors of the Simulium damnosum complex were recorded and their impact on O. volvulus transmission success evaluated. With mitochondrial DNA markers we unambiguously confirmed the presence of infective O. volvulus larvae in vectors from the Sudan savannah region (mean Annual Transmission Potential 2009–2012: 98, range 47–221), but not from the Adamawa highland region. Transmission rates of O. ochengi, a parasite of Zebu cattle, were high in both foci.

          Conclusions/significance

          The high cattle livestock density in conjunction with the high transmission rates of the bovine filaria O. ochengi prevents the transmission of O. volvulus on the Adamawa plateau, whereas transmission in a former hyperendemic focus was markedly reduced, but not completely interrupted after 25 years of ivermectin control. This study may be helpful to gauge the impact of the presence of animal-filariae for O. volvulus transmission in terms of the growing human and livestock populations in sub-Saharan countries.

          Author Summary

          Over the past decades the Fight against river blindness, a tropical disease caused by a nematode worm, has been relatively successful, and a number of countries have been reported to be free of parasite transmission. In North Cameroon, we checked the occurrence of infective stages of Onchocerca volvulus in the transmitting black fly populations for more than three years and were able to confirm that the transmission there is low, but not yet interrupted. In a second location on a highland plateau, however, no infective stages of the human parasite were found. Instead, a closely-related parasite of cattle was present in both places. Given that the areas are not far away from each other and the biting frequencies of the black fly populations are similar, the historically earlier and higher density of cattle herds in one of the regions would explain why it is now free of the parasite due to the effects called zooprophylaxis and cross-reacting premunition. Changes in the socio-economic environment, especially the increase of human and cattle populations have a strong influence on the spread of river blindness in Africa.

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          Most cited references 36

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          Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria.

           T S Detinova (1961)
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            Control of onchocerciasis in Africa: threshold shifts, breakpoints and rules for elimination.

            Control of onchocerciasis in Africa is currently based on annual community-directed treatment with ivermectin (CDTI) which has been assumed to be not efficient enough to bring about elimination. However, elimination has recently been reported to have been achieved by CDTI alone in villages of Senegal and Mali, reviving debate on the eradicability of onchocerciasis in Africa. We investigate the eradicability of onchocerciasis by examining threshold shifts and breakpoints predicted by a stochastic transmission model that has been fitted extensively to data. We show that elimination based on CDTI relies on shifting the threshold biting rate to a level that is higher than the annual biting rate. Breakpoints become relevant in the context of when to stop CDTI. In order for the model to predict a good chance for CDTI to eliminate onchocerciasis, facilitating factors such as the macrofilaricidal effect of ivermectin must be assumed. A chart predicting the minimum efficacy of CDTI required for elimination, dependent on the annual biting rate, is provided. Generalisable recommendations into strategies for the elimination of onchocerciasis are derived, particularly referring to the roles of vectors, the residual infection rate under control, and a low-spreader problem originating from patients with low parasite burdens. Copyright © 2011 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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              Interruption of Onchocerca volvulus transmission in the Abu Hamed focus, Sudan.

              Abu Hamed, Sudan, the northernmost location of onchocerciasis in the world, began community-directed treatment with ivermectin (CDTI) in 1998, with annual treatments enhanced to semiannual in 2007. We assessed the status of the parasite transmission in 2011 entomologically, parasitologically, and serologically. O-150 pool screening showed no parasite DNA in 17,537 black flies collected in 2011 (95% confidence interval upper limit [95% CI UL] = 0.023). Skin microfilariae, nodules, and signs of skin disease were absent in 536 individuals in seven local communities. Similarly, no evidence of Onchocerca volvulus Ov16 antibodies was found in 6,756 school children ≤ 10 years (95% CI UL = 0.03%). Because this assessment of the focus meets the 2001 World Health Organization (WHO) criteria for interrupted transmission, treatment was halted in 2012, and a post-treatment surveillance period was initiated in anticipation of declaration of disease elimination in this area. We provide the first evidence in East Africa that long-term CDTI alone can interrupt transmission of onchocerciasis.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                29 February 2016
                February 2016
                : 10
                : 2
                Affiliations
                [1 ]Institute of Evolution and Ecology, Department of Comparative Zoology, University of Tübingen, Tübingen, Germany
                [2 ]Programme Onchocercoses field station of the University of Tübingen, Ngaoundéré, Cameroon
                [3 ]Veterinary research laboratory, Institute of Agricultural Research for Development, Wakwa Regional Centre, Ngaoundéré, Cameroon
                Common Heritage Foundation, NIGERIA
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AR AE MDA. Performed the experiments: AE AR. Analyzed the data: AE AR. Contributed reagents/materials/analysis tools: AR MDA. Wrote the paper: AE AR MDA.

                Article
                PNTD-D-15-01107
                10.1371/journal.pntd.0004392
                4771805
                26926855
                © 2016 Eisenbarth et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 6, Tables: 1, Pages: 16
                Product
                Funding
                This study was funded by the German Research Foundation under the project number DFG RE-1536/ff. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Nematoda
                Onchocerca
                Onchocerca Volvulus
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Mammals
                Bovines
                Cattle
                Biology and Life Sciences
                Agriculture
                Livestock
                Cattle
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Mammals
                Ruminants
                Cattle
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Onchocerciasis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Onchocerciasis
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Larvae
                Earth Sciences
                Marine and Aquatic Sciences
                Bodies of Water
                Rivers
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Rivers
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Rivers
                People and Places
                Geographical Locations
                Africa
                Cameroon
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Nematoda
                Onchocerca
                Medicine and Health Sciences
                Infectious Diseases
                Vector-Borne Diseases
                Custom metadata
                All relevant data are within the paper and its Supporting Information files. The entomological data prior 2009 (Simulium damnosum s.l. Monthly and Annual Biting Rates and Onchocerca Transmission Potentials from 1976 to 2008) is available on our project website: http://www.riverblindness.eu/epidemiology/fly-catching-sites-data/

                Infectious disease & Microbiology

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