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      Evaluation of a Community-Based Trapping Program to Collect Simulium ochraceum sensu lato for Verification of Onchocerciasis Elimination

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          Abstract

          Background

          Collection of the black fly vectors of onchocerciasis worldwide relies upon human landing collections. Recent studies have suggested that the Esperanza Window Trap baited with a human scent lure and CO 2 had the potential to replace human hosts for the collection of Simulium ochraceum sensu lato in Southern Chiapas focus, Mexico. The feasibility of utilizing these traps in a community-based approach for the collection of S. ochraceum s.l. was evaluated.

          Methodology/Principal findings

          Local residents of a formerly endemic extra-sentinel community for onchocerciasis were trained to carry out collections using the traps. The residents operated the traps over a 60-day period and conducted parallel landing collections, resulting in a total of 28,397 vector black flies collected. None of the flies collected were found to contain parasite DNA when tested by a polymerase chain reaction assay targeting a parasite specific sequence, resulting in a point estimate of infection in the vectors of zero, with an upper bound of the 95% confidence interval 0.13 per 2,000. This meets the accepted criterion for demonstrating an interruption of parasite transmission.

          Conclusions/Significance

          These data demonstrate that Esperanza Window Traps may be effectively operated by minimally trained residents of formerly endemic communities, resulting in the collection of sufficient numbers of flies to verify transmission interruption of onchocerciasis. The traps represent a viable alternative to using humans as hosts for the collection of vector flies as part of the verification of onchocerciasis elimination.

          Author Summary

          Onchocerciasis, or river blindness, is a neglected tropical disease that has been identified by the international community as a candidate for elimination. Both the criteria for verification of elimination and for post-treatment surveillance developed by the international community rely heavily on the use of entomological metrics. Large numbers of vector black flies must be collected to satisfy these metrics. The current standard method for collection of vector black flies for this purpose is human landing collections, is both inefficient and potentially hazardous to the collectors. Here, we report studies evaluating a community-based trial of an inexpensive trap made largely from locally available materials for the replacement of fly collection teams. Traps were provided to residents of a formerly onchocerciasis endemic community in Mexico, and the residents allowed to operate the traps over a 60 day period. The number of flies collected was sufficient to meet the current international criteria necessary to verify that the community was free of O. volvulus transmission. These findings suggest that community based operation of this simple trap might replace human landing collections in the process of verifying the interruption of transmission of onchocerciasis.

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          Most cited references 19

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          Elimination of human onchocerciasis: history of progress and current feasibility using ivermectin (Mectizan(®)) monotherapy.

          We review and analyze approaches over a 65 year period that have proven successful for onchocerciasis control in several different epidemiological settings. These include vector control with the goal of transmission interruption versus the use of mass drug administration using ivermectin (Mectizan(®)) monotherapy. Ivermectin has proven exceedingly effective because it is highly efficacious against Onchocerca volvulus microfilariae, the etiological agent of onchocercal skin and ocular disease and the infective stage for the vector. For these reasons, the drug was donated by the Merck Company for regional control programs in Africa and the Americas. Recurrent treatment with ivermectin at semi-annual intervals also impacts adult worms and result in loss of fecundity and increased mortality. Using a strategy of 6-monthly treatments with high coverage rates, the Onchocerciasis Elimination Program for the Americas has interrupted transmission in seven of the thirteen foci in the Americas and is on track to eliminate onchocerciasis in the region by 2015. Treatments given annually or semi-annually for 15-17 years in three hyperendemic onchocerciasis foci in Mali and Senegal also have resulted in a few infections in the human population with transmission levels below thresholds postulated for elimination. Follow-up evaluations did not detect any recrudescence of infection or transmission, suggesting that onchocerciasis elimination could be feasible with Mectizan(®) treatment in some endemic foci in Africa. Copyright © 2010 Elsevier B.V. All rights reserved.
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            The Onchocerciasis Elimination Program for the Americas (OEPA).

             M Sauerbrey (2008)
            Human onchocerciasis (river blindness) occurs in 13 foci distributed among six countries in Latin America (Brazil, Colombia, Ecuador, Guatemala, Mexico and Venezuela), where about 500,000 people are considered at risk. An effort to eliminate the disease from the region was launched in response to a specific resolution adopted by the PanAmerican Health Organization (PAHO) in 1991: to eliminate onchocerciasis from the region, as a public-health problem, by 2007. The effort took advantage of the donation of the drug Mectizan (ivermectin) by Merck & Co., Inc. In 1992, the Onchocerciasis Elimination Program for the Americas (OEPA) was launched, with its headquarters in Guatemala, to act as a technical and co-ordinating body of a multinational, multi-agency coalition that includes the endemic countries, PAHO, The Carter Center, Lions Clubs, the United States Centers for Disease Control and Prevention, The Bill and Melinda Gates Foundation, Merck & Co., Inc., and other partners. This public-private partnership facilitated the establishment of programmes for the semi-annual mass administration of Mectizan in the six countries with onchocerciasis. The aims were to (1) provide sustained treatments, with coverage reaching at least 85% of those eligible to receive the drug (in the 1845 endemic communities that are distributed within the 13 regional foci); (2) eliminate new morbidity caused by Onchocerca volvulus infection by 2007; and (3) eliminate transmission of the parasite wherever feasible. Significant progress has already been made in all six countries, each of which has active programmes with treatment coverages exceeding the target of 85%. The progress is being documented in accordance with certification guidelines for onchocerciasis elimination established by the World Health Organization. No new cases of onchocercal blindness are being reported in the region, and ocular disease attributable to O. volvulus has been eliminated from nine of the 13 foci. Treatment is no longer needed in Santa Rosa, Guatemala, where transmission has been eliminated, and will be halted in at least three other foci in 2008, as they confirm the interruption of transmission. Treatment efforts should now be concentrated on the five foci where significant transmission remains: Central (Guatemala), Amazonas/Roraima (Brazil), North-central (Venezuela), North-east (Venezuela) and South (Venezuela). Based upon the experience gained, the well-established operations and the success achieved so far, it seems reasonable to estimate that onchocerciasis could be eliminated from most of the remaining foci in the Americas by 2012. The protocol, criteria and deadline for stopping all onchocerciasis treatment in the region should soon be addressed by OEPA's Program Co-ordinating Committee (PCC), in co-ordination with the PAHO.
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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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                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
                October 2014
                23 October 2014
                : 8
                : 10
                Affiliations
                [1 ]Centro de Biotecnología Genómica, Instituto Politécnico Nacional, Reynosa, Tamaulipas, México
                [2 ]Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey, Nuevo León, México
                [3 ]Public Health Entomology and Parasitology Unit, Department of Biological Sciences, Osun State University, Osogbo, Nigeria
                [4 ]Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, United States of America
                [5 ]Global Health Infectious Disease Research Program, Department of Global Health, University of South Florida, Tampa, Florida, United States of America
                Technical University of Mombasa, Kenya
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MARP EWC TRU. Performed the experiments: MARP MAA ICRL. Analyzed the data: MARP TRU EWC. Wrote the paper: MARP EWC TRU.

                Article
                PNTD-D-14-00747
                10.1371/journal.pntd.0003249
                4207651
                25340517

                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
                Pages: 6
                Funding
                This research was funded by a grant from The Bill & Melinda Gates Foundation (Project OPP1017870). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Onchocerciasis
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology

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