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      Status of Onchocerciasis Transmission after More Than a Decade of Mass Drug Administration for Onchocerciasis and Lymphatic Filariasis Elimination in Central Nigeria: Challenges in Coordinating the Stop MDA Decision

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          Abstract

          Background

          This study was undertaken in five onchocerciasis/lymphatic filariasis (LF) co-endemic local government areas (LGAs) in Plateau and Nasarawa, Nigeria. Annual MDA with ivermectin had been given for 17 years, 8 of which were in combination with albendazole. In 2008, assessments indicated that LF transmission was interrupted, but that the MDA had to continue due to the uncertain status of onchocerciasis transmission. Accordingly, assessments to determine if ivermectin MDA for onchocerciasis could be stopped were conducted in 2009.

          Methods

          We evaluated nodule, microfilarial (mf) skin snip, and antibody (IgG4 response to OV16) prevalence in adults and children in six sentinel sites where baseline data from the 1990s were available. We applied the 2001 WHO criteria for elimination of onchocerciasis that defined transmission interruption as an infection rate of <0.1% in children (using both skin snip and OV16 antibody) and a rate of infective (L3) blackflies of <0.05%.

          Results

          Among adult residents in sentinel sites, mean mf prevalence decreased by 99.37% from the 1991–1993 baseline of 42.95% (64/149) to 0.27% (2/739) in 2009 (p<0.001). The OV16 seropositivity of 3.52% (26/739) among this same group was over ten times the mf rate. No mf or nodules were detected in 4,451 children in sentinel sites and ‘spot check’ villages, allowing the exclusion of 0.1% infection rate with 95% confidence. Seven OV16 seropositives were detected, yielding a seroprevalence of 0.16% (0.32% upper 95%CI). No infections were detected in PCR testing of 1,568 Simulium damnosum s.l. flies obtained from capture sites around the six sentinel sites.

          Conclusion

          Interruption of transmission of onchocerciasis in these five LGAs is highly likely, although the number of flies caught was insufficient to exclude 0.05% with 95% confidence (upper CI 0.23%). We suggest that ivermectin MDA could be stopped in these LGAs if similar results are seen in neighboring districts.

          Author Summary

          Both lymphatic filariasis and onchocerciasis are treated with ivermectin-based mass drug administration (MDA) regimens in Africa. Where the infections are co-endemic, ivermectin treatments cannot be stopped until both infection transmission cycles are broken. This report follows a previous determination that the LF transmission cycle had been interrupted in five districts (LGAs in Nigeria) but evidence was needed on the status of the onchocerciasis transmission cycle prior to halting MDA. In this report we determined (based on WHO guidelines) that most likely the transmission of onchocerciasis has been interrupted in Plateau and Nasarawa States and we conclude that ivermectin MDA could be stopped.

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          Most cited references8

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          Transmission of Onchocerciasis in Wadelai Focus of Northwestern Uganda Has Been Interrupted and the Disease Eliminated

          Wadelai, an isolated focus for onchocerciasis in northwest Uganda, was selected for piloting an onchocerciasis elimination strategy that was ultimately the precursor for countrywide onchocerciasis elimination policy. The Wadelai focus strategy was to increase ivermectin treatments from annual to semiannual frequency and expand geographic area in order to include communities with nodule rate of less than 20%. These communities had not been covered by the previous policy that sought to control onchocerciasis only as a public health problem. From 2006 to 2010, Wadelai program successfully attained ultimate treatment goal (UTG), treatment coverage of ≥90%, despite expanding from 19 to 34 communities and from 5,600 annual treatments to over 29,000 semiannual treatments. Evaluations in 2009 showed no microfilaria in skin snips of over 500 persons examined, and only 1 of 3011 children was IgG4 antibody positive to the OV16 recombinant antigen. No Simulium vectors were found, and their disappearance could have sped up interruption of transmission. Although twice-per-year treatment had an unclear role in interruption of transmission, the experience demonstrated that twice-per-year treatment is feasible in the Ugandan setting. The monitoring data support the conclusion that onchocerciasis has been eliminated from the Wadelai focus of Uganda.
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            Elimination of Onchocercia volvulus transmission in the Santa Rosa focus of Guatemala.

            To eliminate transmission of Onchocerca volvulus, semiannual mass treatment with ivermectin (Mectizan; donated by Merck & Co) has been underway in Guatemala since 2000. We applied the 2001 World Health Organization (WHO) elimination criteria in the Santa Rosa focus of onchocerciasis transmission in Guatemala (10,923 persons at risk). No evidence of parasite DNA was found in 2,221 Simulium ochraceum vectors (one-sided 95% confidence interval [CI], 0-0.086%), and no IgG4 antibody positives to recombinant antigen OV16 were found in a sample of 3,232 school children (95% CI, 0-0.009%). We also found no evidence of microfilariae in the anterior segment of the eye in 363 area residents (95% CI, 0-0.08%). Our interpretation of these data, together with historical information, suggest that transmission of O. volvulus is permanently interrupted in Santa Rosa and that ivermectin treatments there can be halted.
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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, USA )
                1935-2727
                1935-2735
                September 2014
                18 September 2014
                : 8
                : 9
                : e3113
                Affiliations
                [1 ]The Carter Center, Atlanta, Georgia, United States of America
                [2 ]The Carter Center Nigeria, Jos, Plateau, Nigeria
                [3 ]University of Jos, Plateau, Nigeria
                [4 ]Consultant, River Blindness Foundation, Atlanta, Georgia, United States of America
                [5 ]Plateau State Ministry of Health, Jos, Plateau, Nigeria
                [6 ]Nasarawa State Ministry of Health, Lafia, Nasarawa, Nigeria
                [7 ]Department of Public Health, Federal Ministry of Health, Abuja, FCT, Nigeria
                Noguchi Memorial Institute for Medical Research, Ghana
                Author notes

                I have read the journal's policy and have the following conflicts: Donations of albendazole from GlaxoSmithKline and Mectizan (ivermectin) from Merck & Co. were facilitated through the Mectizan Donation program. This does not alter our adherence to all PLOS NTDs policies on sharing data and materials.

                Conceived and designed the experiments: DSE KA JU AE CGP EM YS BO FOR. Performed the experiments: KA JU AE CGP WA HM EP CU. Analyzed the data: DSE WA KA EP CU. Contributed reagents/materials/analysis tools: BO YS EM. Wrote the paper: DSE FOR JU AE EM HM CGP WA EP CU YS BO.

                † Deceased.

                Article
                PNTD-D-13-01761
                10.1371/journal.pntd.0003113
                4169246
                25233351
                9cf1f945-a8c1-4150-abb5-1e806150025b
                Copyright @ 2014

                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.

                History
                : 25 October 2013
                : 13 July 2014
                Page count
                Pages: 10
                Funding
                GlaxoSmithKline provided albendazole, and Merck & Co. provided ivermectin through the Mectizan Donation Program. Early support of MDA was provided by the River Blindness Foundation and Mr. Johm Moores. Later support for the program and this research came from the Bill & Melinda Gates Foundation. The funders had no role in study design, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Infectious Disease Epidemiology
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Filariasis
                Lymphatic Filariasis
                Onchocerciasis
                Epidemiology
                Public and Occupational Health
                Global Health
                Infectious Diseases
                Tropical Diseases
                Neglected Tropical Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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