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      Characterizing the malaria rural-to-urban transmission interface: The importance of reactive case detection

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          Abstract

          Background

          Reported urban malaria cases are increasing in Latin America, however, evidence of such trend remains insufficient. Here, we propose an integrated approach that allows characterizing malaria transmission at the rural-to-urban interface by combining epidemiological, entomological, and parasite genotyping methods.

          Methods/Principal findings

          A descriptive study that combines active (ACD), passive (PCD), and reactive (RCD) case detection was performed in urban and peri-urban neighborhoods of Quibdó, Colombia. Heads of households were interviewed and epidemiological surveys were conducted to assess malaria prevalence and identify potential risk factors. Sixteen primary cases, eight by ACD and eight by PCD were recruited for RCD. Using the RCD strategy, prevalence of 1% by microscopy (6/604) and 9% by quantitative polymerase chain reaction (qPCR) (52/604) were found. A total of 73 houses and 289 volunteers were screened leading to 41 secondary cases, all of them in peri-urban settings (14% prevalence). Most secondary cases were genetically distinct from primary cases indicating that there were independent occurrences. Plasmodium vivax was the predominant species (76.3%, 71/93), most of them being asymptomatic (46/71). Urban and peri-urban neighborhoods had significant sociodemographic differences. Twenty-four potential breeding sites were identified, all in peri-urban areas. The predominant vectors for 1,305 adults were Anopheles nuneztovari (56,2%) and An. Darlingi (42,5%). One An. nuneztovari specimen was confirmed naturally infected with P. falciparum by ELISA.

          Conclusions

          This study found no evidence supporting the existence of urban malaria transmission in Quibdó. RCD strategy was more efficient for identifying malaria cases than ACD alone in areas where malaria transmission is variable and unstable. Incorporating parasite genotyping allows discovering hidden patterns of malaria transmission that cannot be detected otherwise. We propose to use the term “focal case” for those primary cases that lead to discovery of secondary but genetically unrelated malaria cases indicating undetected malaria transmission.

          Author summary

          Malaria is a disease of rural areas in developing countries. Although a rise in urban malaria cases has been noted during the last decade, this trend could be an artifact due to lack of solid data. In order to better understand “urban” and “peri-urban” malaria, we developed a rigorous and systematic methodology that allows characterizing malaria risk in such settings. Our approach is based on cross-sectional studies using active and reactive case detection strategies, genotyping of parasite isolates in order to better understand transmission patterns, and the local assessment of the entomological factors that allow active transmission in urban and peri-urban neighborhoods. This approach was tested in Quibdó, Colombia. No evidence of malaria transmission in urban areas was found. However, we found solid evidence indicating transmission in peri-urban areas due to Plasmodium vivax (86%). This was supported by the identification of Anopheles mosquitoes and their breeding places. Our results show that reactive case detection is not only an effective strategy to identify cases in areas where transmission is variable and unstable, but also allows the detection of hidden transmission when combined with genotyping methods. Such patterns are undetected by traditional surveillance methods.

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          Most cited references 30

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          Malaria transmission in urban sub-Saharan Africa.

          The rapid increase in the world's urban population has major implications for the epidemiology of malaria. A review of malaria transmission in sub-Saharan African cities shows the strong likelihood of transmission occurring within these sprawling cities, whatever the size or characteristics of their bioecologic environment. A meta-analysis of results from studies of malaria transmission in sub-Saharan Africa shows a loose linear negative relationship between mean annual entomologic inoculation rates (EIR) and the level of urbanicity. Few studies have failed to find entomologic evidence of some transmission. Our results show mean annual EIRs of 7.1 in the city centers, 45.8 in periurban areas, and 167.7 in rural areas. The impact of urbanization in reducing transmission is more marked in areas where the mean rainfall is low and seasonal. Considerable variation in the level of transmission exists among cities and within different districts in the same city. This article presents evidence from past literature to build a conceptual framework to begin to explain this heterogeneity. The potential for malaria epidemics owing to decreasing levels of natural immunity may be offset by negative impacts of urbanization on the larval ecology of anopheline mosquitoes. Malaria control in urban environments may be simpler as a result of urbanization; however, much of what we know about malaria transmission in rural environments might not hold in the urban context.
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            Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays.

            There have been reports of increasing numbers of cases of malaria among migrants and travelers. Although microscopic examination of blood smears remains the "gold standard" in diagnosis, this method suffers from insufficient sensitivity and requires considerable expertise. To improve diagnosis, a multiplex real-time PCR was developed. One set of generic primers targeting a highly conserved region of the 18S rRNA gene of the genus Plasmodium was designed; the primer set was polymorphic enough internally to design four species-specific probes for P. falciparum, P. vivax, P. malarie, and P. ovale. Real-time PCR with species-specific probes detected one plasmid copy of P. falciparum, P. vivax, P. malariae, and P. ovale specifically. The same sensitivity was achieved for all species with real-time PCR with the 18S screening probe. Ninety-seven blood samples were investigated. For 66 of them (60 patients), microscopy and real-time PCR results were compared and had a crude agreement of 86% for the detection of plasmodia. Discordant results were reevaluated with clinical, molecular, and sequencing data to resolve them. All nine discordances between 18S screening PCR and microscopy were resolved in favor of the molecular method, as were eight of nine discordances at the species level for the species-specific PCR among the 31 samples positive by both methods. The other 31 blood samples were tested to monitor the antimalaria treatment in seven patients. The number of parasites measured by real-time PCR fell rapidly for six out of seven patients in parallel to parasitemia determined microscopically. This suggests a role of quantitative PCR for the monitoring of patients receiving antimalaria therapy.
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              Urbanization in sub-saharan Africa and implication for malaria control.

              Malaria not only remains a leading cause of morbidity and mortality, but it also impedes socioeconomic development, particularly in sub-Saharan Africa. Rapid and unprecedented urbanization, going hand-in-hand with often declining economies, might have profound implications for the epidemiology and control of malaria, as the relative disease burden increases among urban dwellers. Reviewing the literature and using a modeling approach, we find that entomologic inoculation rates in cities range from 0 to 54 per year, depending on the degree of urbanization, the spatial location within a city, and overall living conditions. Using the latest United Nations figures on urbanization prospects, nighttime light remotely sensed images, and the "Mapping Malaria Risk in Africa" results on climate suitability for stable malaria transmission, we estimate that 200 million people (24.6% of the total African population) currently live in urban settings where they are at risk of contracting the disease. Importantly, the estimated total surface area covered by these urban settings is only approximately 1.1-1.6% of the total African surface. Considering different plausible scenarios, we estimate an annual incidence of 24.8-103.2 million cases of clinical malaria attacks among urban dwellers in Africa. These figures translate to 6-28% of the estimated global annual disease incidence. Against this background, basic health care delivery systems providing early diagnosis and early treatment and preventive actions through mother and child health programs and the promotion of insecticide-treated bed nets for the rapidly growing numbers of the urban poor must be improved alongside well-tailored and integrated malaria control strategies. We propose environmental management and larviciding within well-specified productive sites as a main feature for such an integrated control approach. Mitigation of the current burden of malaria in urban African settings, in turn, is a necessity for stimulating environmentally and socially sustainable development. Copyright 2004 The American Society of Tropical Medicine and Hygiene
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: InvestigationRole: Writing – original draft
                Role: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                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
                17 July 2017
                July 2017
                : 11
                : 7
                Affiliations
                [1 ] Malaria Vaccine and Drug Development Center, Cali, Colombia
                [2 ] Ministerio de Salud y Protección Social de Colombia, Bogotá, Colombia
                [3 ] Instituto Nacional de Salud de Colombia, Bogotá, Colombia
                [4 ] Department of Biology/Institute for Genomics and Evolutionary Medicine (iGEM), Temple University, Philadelphia- Pennsylvania, United States of America
                [5 ] Caucaseco Scientific Research Center, Cali, Colombia
                [6 ] School of bacteriology and clinical laboratory, Faculty of Health, Universidad del Valle, Cali, Colombia
                Common Heritage Foundation, NIGERIA
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-17-00532
                10.1371/journal.pntd.0005780
                5531679
                28715415
                © 2017 Molina Gómez 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: 3, Tables: 2, Pages: 15
                Product
                Funding
                Funded by: NIH/NIAID
                Award ID: 5U19AI089702
                Award Recipient :
                This research was performed in the context of the Latin American Malaria Research Center, ICEMRs, NIH/NIAID (5U19AI089702). 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
                Malaria
                Medicine and Health Sciences
                Tropical Diseases
                Malaria
                Biology and Life Sciences
                Parasitology
                Parasite Groups
                Apicomplexa
                Plasmodium
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Earth Sciences
                Geography
                Human Geography
                Neighborhoods
                Social Sciences
                Human Geography
                Neighborhoods
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Genotyping
                Research and Analysis Methods
                Molecular Biology Techniques
                Genotyping
                Earth Sciences
                Geography
                Geographic Areas
                Urban Areas
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-07-27
                All relevant data are within the paper.

                Infectious disease & Microbiology

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