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      No Evidence for Lymphatic Filariasis Transmission in Big Cities Affected by Conflict Related Rural-Urban Migration in Sierra Leone and Liberia

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          Abstract

          Background

          In West Africa, the principal vectors of lymphatic filariasis (LF) are Anopheles species with Culex species playing only a minor role in transmission, if any. Being a predominantly rural disease, the question remains whether conflict-related migration of rural populations into urban areas would be sufficient for active transmission of the parasite.

          Methodology/Principal Findings

          We examined LF transmission in urban areas in post-conflict Sierra Leone and Liberia that experienced significant rural-urban migration. Mosquitoes from Freetown and Monrovia, were analyzed for infection with Wuchereria bancrofti. We also undertook a transmission assessment survey (TAS) in Bo and Pujehun districts in Sierra Leone. The majority of the mosquitoes collected were Culex species, while Anopheles species were present in low numbers. The mosquitoes were analyzed in pools, with a maximum of 20 mosquitoes per pool. In both countries, a total of 1731 An. gambiae and 14342 Culex were analyzed for W. bancrofti, using the PCR. Two pools of Culex mosquitoes and 1 pool of An. gambiae were found infected from one community in Freetown. Pool screening analysis indicated a maximum likelihood of infection of 0.004 (95% CI of 0.00012–0.021) and 0.015 (95% CI of 0.0018–0.052) for the An. gambiae and Culex respectively. The results indicate that An. gambiae is present in low numbers, with a microfilaria prevalence breaking threshold value not sufficient to maintain transmission. The results of the TAS in Bo and Pujehun also indicated an antigen prevalence of 0.19% and 0.67% in children, respectively. This is well below the recommended 2% level for stopping MDA in Anopheles transmission areas, according to WHO guidelines.

          Conclusions

          We found no evidence for active transmission of LF in cities, where internally displaced persons from rural areas lived for many years during the more than 10 years conflict in Sierra Leone and Liberia.

          Author Summary

          There have been many arguments regarding the implementation of Mass Drug Administration (MDA) activities for elephantiasis control in urban areas, and especially in countries where the disease is mostly found in rural settings. Blanket MDA in implementation units in big cities, may be costly and unnecessary, without evidence for active transmission in urban areas. Over 1 million people were treated in Freetown during the first MDA carried out in 2010. This represents hundreds of thousands dollars that may serve a better use in reducing the impact of elephantiasis in areas with established on-going transmission. This study was conducted to assess the evidence of transmission of elephantiasis in urban areas, as a result of rural to urban migration in West African countries that have experienced civil wars, and the displacement of people from rural to urban areas. The results showed that the main mosquitoes transmitting elephantiasis are in numbers not enough to support transmission. Testing of individuals also showed very few people to have infection. Together, the results show that elephantiasis infection in the urban areas, where the study was conducted, is not enough to justify the need for MDA in the national capitals. This study represents a strategy that can be adopted in many countries, to inform the decision for undertaking MDA activities in cities.

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          Most cited references31

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          Effect of yearly mass drug administration with diethylcarbamazine and albendazole on bancroftian filariasis in Egypt: a comprehensive assessment.

          Egypt was one of the first countries to implement a national programme to eliminate lymphatic filariasis based on WHO's strategy of repeated rounds of mass drug administration (MDA) with diethylcarbamazine and albendazole (target population, 2.5 million in 181 localities). We assessed the effect of five yearly rounds of MDA on filariasis in four sentinel villages in Egypt. We studied two areas with different infection rates before MDA: the Qalubyia study area had a low infection rate because of previous treatment with diethylcarbamazine; this was typical of most filariasis-endemic villages in Egypt before MDA. The Giza study area had a high baseline infection rate. We undertook repeated surveys in villages for treatment compliance and tests for microfilaraemia and circulating filarial antigenaemia, antibodies to filarial antigen Bm14 in schoolchildren, and infections in indoor-resting mosquitoes (assessed by PCR). MDA compliance rates were excellent (>80%). In Giza after MDA, prevalence rates of microfilaraemia and circulating filarial antigenaemia fell from 11.5% to 1.2%, and from 19.0% to 4.8%, respectively (p<0.0001). Corresponding rates in Qalubyia fell from 3.1% to 0% and 13.6% to 3.1%, respectively (p<0.0001). Rates of antifilarial antibody and circulating filarial antigenaemia in schoolchildren (aged about 7-8 years), fell from 18.3% to 0.2% (p<0.0001) and from 10.0% to 0.4% (p<0.0001) in Giza, respectively, and from 1.7% to 0% and 1.7% to 0% (both p=0.13) in Qalubyia, respectively. Mosquito infection rates fell from 3.07% (95% CI 2.38-3.88) to 0.19% (0.08-0.38) in Giza and from 4.37% (3.07-5.99) to 0% (0-0.05) in Qalubyia. MDA greatly affects variables related to infection (microfilaraemia and circulating filarial antigenaemia prevalence rates) and transmission (antifilarial antibodies in young children and mosquito infection rates). Our results suggest that after five rounds of MDA filariasis is likely to have been eliminated in most endemic localities in Egypt.
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            Determining the prevalence of Onchocerca volvulus infection in vector populations by polymerase chain reaction screening of pools of black flies.

            An important variable in the epidemiology of arthropodborne diseases is the intensity of transmission, which is a function of host-vector contact and the prevalence of infection in the vector population. This latter value is often difficult to estimate. It is possible to envision the application of polymerase chain reaction (PCR) assays to this problem. To accomplish this, the assay must detect a single infected vector in a pool containing a large number of uninfected individuals. It must also be possible to calculate the prevalence of infection from the number of positive pools. A PCR assay for detecting Onchocerca volvulus in pools of vector black flies is described, and an algorithm is presented to calculate the prevalence of infection in the vector population, based upon the proportion of PCR-positive pools. This algorithm should be applicable to any disease for which a PCR assay is available.
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              A critical appraisal of molecular xenomonitoring as a tool for assessing progress toward elimination of Lymphatic Filariasis.

              We used molecular xenomonitoring (MX, detection of filarial DNA in mosquitoes) to evaluate the impact of mass drug administration (MDA) in sentinel locations in Egypt with high (11.5%) and low (4.1%) baseline microfilaria prevalence rates. Blood-fed Culex pipiens were pooled by household and tested for Wuchereria bancrofti DNA by PCR. There was no significant relationship between the infection status of household residents and parasite DNA status of mosquitoes from the same houses. After 5 MDA rounds, parasite DNA rates in mosquitoes in high- and low-prevalence areas were reduced by 93.8% and 100% to 0.19% (95% CI: 0.076-0.382%) and 0% (95% CI: 0-0.045%), respectively. These changes were consistent with decreases in microfilaria prevalence rates in these sites; they provide insight regarding the minimal mosquito DNA rates necessary for sustained transmission of filariasis in Egypt. We conclude that MX is a powerful tool for monitoring the impact of MDA on filariasis endemicity and transmission.
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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
                February 2014
                6 February 2014
                : 8
                : 2
                : e2700
                Affiliations
                [1 ]Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana
                [2 ]Ministry of Health and Sanitation, Freetown, Sierra Leone
                [3 ]Ministry of Health and Social Welfare, Monrovia, Liberia
                [4 ]Mercy Hospital Research Laboratory, Bo, Sierra Leone
                [5 ]Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                [6 ]Liberian Institute for Biomedical Research, Charlesville, Liberia
                Institute of Medical Microbiology, Germany
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MJB BGK SS FKB DKdS KK DAB MPR JBK. Performed the experiments: DKdS MGM CAN SS RA. Analyzed the data: DKdS MJB MPR. Contributed reagents/materials/analysis tools: MJB DAB. Wrote the paper: DKdS MJB CAN BGK SS FKB MGM KK DAB MPR RA JBK.

                Article
                PNTD-D-13-00895
                10.1371/journal.pntd.0002700
                3916318
                24516686
                e98af1ed-737c-4341-9a0a-e82f66c3514a
                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
                : 18 June 2013
                : 4 January 2014
                Page count
                Pages: 6
                Funding
                This study was supported by the Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, through funding from DFID. The funders of this study had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine
                Infectious Diseases
                Neglected Tropical Diseases
                Lymphatic Filariasis
                Vectors and Hosts
                Mosquitoes

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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