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      The Limits and Intensity of Plasmodium falciparum Transmission: Implications for Malaria Control and Elimination Worldwide

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          Abstract

          Background

          The efficient allocation of financial resources for malaria control using appropriate combinations of interventions requires accurate information on the geographic distribution of malaria risk. An evidence-based description of the global range of Plasmodium falciparum malaria and its endemicity has not been assembled in almost 40 y. This paper aims to define the global geographic distribution of P. falciparum malaria in 2007 and to provide a preliminary description of its transmission intensity within this range.

          Methods and Findings

          The global spatial distribution of P. falciparum malaria was generated using nationally reported case-incidence data, medical intelligence, and biological rules of transmission exclusion, using temperature and aridity limits informed by the bionomics of dominant Anopheles vector species. A total of 4,278 spatially unique cross-sectional survey estimates of P. falciparum parasite rates were assembled. Extractions from a population surface showed that 2.37 billion people lived in areas at any risk of P. falciparum transmission in 2007. Globally, almost 1 billion people lived under unstable, or extremely low, malaria risk. Almost all P. falciparum parasite rates above 50% were reported in Africa in a latitude band consistent with the distribution of Anopheles gambiae s.s. Conditions of low parasite prevalence were also common in Africa, however. Outside of Africa, P. falciparum malaria prevalence is largely hypoendemic (less than 10%), with the median below 5% in the areas surveyed.

          Conclusions

          This new map is a plausible representation of the current extent of P. falciparum risk and the most contemporary summary of the population at risk of P. falciparum malaria within these limits. For 1 billion people at risk of unstable malaria transmission, elimination is epidemiologically feasible, and large areas of Africa are more amenable to control than appreciated previously. The release of this information in the public domain will help focus future resources for P. falciparum malaria control and elimination.

          Abstract

          Combining extensive surveillance and climate data, as well as biological characteristics of Anopheles mosquitoes, Robert Snow and colleagues create a global map of risk for P. falciparum malaria.

          Editors' Summary

          Background.

          Malaria is a parasitic disease that occurs in tropical and subtropical regions of the world. 500 million cases of malaria occur every year, and one million people, mostly children living in sub-Saharan Africa, die as a result. The parasite mainly responsible for these deaths— Plasmodium falciparum—is transmitted to people through the bites of infected mosquitoes. These insects inject a life stage of the parasite called sporozoites, which invade and reproduce in human liver cells. After a few days, the liver cells release merozoites (another life stage of the parasite), which invade red blood cells. Here, they multiply before bursting out and infecting more red blood cells, causing fever and damaging vital organs. Infected red blood cells also release gametocytes, which infect mosquitoes when they take a human blood meal. In the mosquito, the gametocytes multiply and develop into sporozoites, thus completing the parasite's life cycle. Malaria can be treated with antimalarial drugs and can be prevented by controlling the mosquitoes that spread the parasite (for example, by using insecticides) and by avoiding mosquito bites (for example, by sleeping under a insecticide-treated bednet).

          Why Was This Study Done?

          Because malaria poses such a large global public-health burden, many national and international agencies give countries where malaria is endemic (always present) financial resources for malaria control and, where feasible, elimination. The efficient allocation of these resources requires accurate information on the geographical distribution of malaria risk, but it has been 40 years since a map of malaria risk was assembled. In this study, which is part of the Malaria Atlas Project, the researchers have generated a new global map to show where the risk of P. falciparum transmission is moderate or high (stable transmission areas where malaria is endemic) and areas where the risk of transmission is low (unstable transmission areas where sporadic outbreaks of malaria occur).

          What Did the Researchers Do and Find?

          To construct their map of P. falciparum risk, the researchers collected nationally reported data on malaria cases each year and on the number of people infected in sampled communities. They also collected information about climatic conditions that affect the parasite's life cycle and consequently the likelihood of active transmission. For example, below a certain temperature, infected mosquitoes reach the end of their natural life span before the parasite has had time to turn into infectious sporozoites, which means that malaria transmission does not occur. By combining these different pieces of information with global population data, the researchers calculated that 2.37 billion people (about 35% of the world's population) live in areas where there is some risk of P. falciparum transmission, and that about 1 billion of these people live where there is a low but still present risk of malaria transmission. Furthermore, nearly all the regions where more than half of children carry P. falciparum parasites (a P. falciparum prevalence of more than 50%) are in Africa, although there are some African regions where few people are infected with P. falciparum. Outside Africa, the P. falciparum prevalence is generally below 5%.

          What Do These Findings Mean?

          The accuracy of this new map of the spatial distribution of P. falciparum malaria risk depends on the assumptions made in its assembly and the accuracy of the data fed into it. Nevertheless, by providing a contemporary indication of global patterns of P. falciparum malaria risk, this new map should be a valuable resource for agencies that are trying to control and eliminate malaria. (A similar map for the more common but less deadly P. vivax malaria would also be useful, but has not yet been constructed because less information is available and its biology is more complex.) Importantly, the map provides an estimate of the number of people who are living in areas where malaria transmission is low, areas where it should, in princple, be possible to use existing interventions to eliminate the parasite. In addition, it identifies large regions of Africa where the parasite might be more amenable to control and, ultimately, elimination than previously thought. Finally, with regular updates, this map will make it possible to monitor the progress of malaria control and elimination efforts.

          Additional Information.

          Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0050038.

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          Most cited references62

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          The global distribution of clinical episodes of Plasmodium falciparum malaria.

          Interest in mapping the global distribution of malaria is motivated by a need to define populations at risk for appropriate resource allocation and to provide a robust framework for evaluating its global economic impact. Comparison of older and more recent malaria maps shows how the disease has been geographically restricted, but it remains entrenched in poor areas of the world with climates suitable for transmission. Here we provide an empirical approach to estimating the number of clinical events caused by Plasmodium falciparum worldwide, by using a combination of epidemiological, geographical and demographic data. We estimate that there were 515 (range 300-660) million episodes of clinical P. falciparum malaria in 2002. These global estimates are up to 50% higher than those reported by the World Health Organization (WHO) and 200% higher for areas outside Africa, reflecting the WHO's reliance upon passive national reporting for these countries. Without an informed understanding of the cartography of malaria risk, the global extent of clinical disease caused by P. falciparum will continue to be underestimated.
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            Urbanization, malaria transmission and disease burden in Africa.

            Many attempts have been made to quantify Africa's malaria burden but none has addressed how urbanization will affect disease transmission and outcome, and therefore mortality and morbidity estimates. In 2003, 39% of Africa's 850 million people lived in urban settings; by 2030, 54% of Africans are expected to do so. We present the results of a series of entomological, parasitological and behavioural meta-analyses of studies that have investigated the effect of urbanization on malaria in Africa. We describe the effect of urbanization on both the impact of malaria transmission and the concomitant improvements in access to preventative and curative measures. Using these data, we have recalculated estimates of populations at risk of malaria and the resulting mortality. We find there were 1,068,505 malaria deaths in Africa in 2000 - a modest 6.7% reduction over previous iterations. The public-health implications of these findings and revised estimates are discussed.
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              Determining global population distribution: methods, applications and data.

              Evaluating the total numbers of people at risk from infectious disease in the world requires not just tabular population data, but data that are spatially explicit and global in extent at a moderate resolution. This review describes the basic methods for constructing estimates of global population distribution with attention to recent advances in improving both spatial and temporal resolution. To evaluate the optimal resolution for the study of disease, the native resolution of the data inputs as well as that of the resulting outputs are discussed. Assumptions used to produce different population data sets are also described, with their implications for the study of infectious disease. Lastly, the application of these population data sets in studies to assess disease distribution and health impacts is reviewed. The data described in this review are distributed in the accompanying DVD.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Med
                pmed
                plme
                plosmed
                PLoS Medicine
                Public Library of Science (San Francisco, USA )
                1549-1277
                1549-1676
                February 2008
                26 February 2008
                : 5
                : 2
                : e38
                Affiliations
                [1 ] Malaria Public Health and Epidemiology Group, Centre for Geographic Medicine, Kenyan Medical Research Institute–University of Oxford–Wellcome Trust Collaborative Programme, Nairobi, Kenya
                [2 ] Spatial Ecology and Epidemiology Group, Department of Zoology, University of Oxford, Oxford, United Kingdom
                [3 ] Centre for Tropical Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
                [4 ] Department of Zoology and Emerging Pathogens Institute, University of Florida, Gainesville, Florida, United States of America
                Royal Melbourne Hospital, Australia
                Author notes
                * To whom correspondence should be addressed. E-mail: shay@ 123456nairobi.kemri-wellcome.org (SIH); rsnow@ 123456nairobi.kemri-wellcome.org (RWS)
                Article
                07-PLME-RA-1649R2 plme-05-02-17
                10.1371/journal.pmed.0050038
                2253602
                18303939
                3c7c96df-6243-450a-9013-6027ce1b98d4
                Copyright: © 2008 Guerra 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.
                History
                : 2 October 2007
                : 21 December 2007
                Page count
                Pages: 12
                Categories
                Research Article
                Infectious Diseases
                Public Health and Epidemiology
                Malaria
                International Health
                Travel Medicine
                Medicine in Developing Countries
                Infectious Diseases
                Custom metadata
                Guerra CA, Gikandi PW, Tatem AJ, Noor AM, Smith DL, et al. (2008) The limits and intensity of Plasmodium falciparum transmission: Implications for malaria control and elimination worldwide. PLoS Med 5(2): e38. doi: 10.1371/journal.pmed.0050038

                Medicine
                Medicine

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