31
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Mosquito feeding behavior and how it influences residual malaria transmission across Africa

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Significance

          Malaria transmission persists even when mosquito control is used effectively. This “residual transmission” measures all forms of transmission that are beyond the reach of standard insecticidal nets and indoor residual spraying of insecticides when used optimally. The epidemiological importance of the time of day mosquitoes bite and how much this contributes to residual transmission is unclear. The scale of the problem must be understood to demonstrate the need for outdoor vector control tools. An additional 10.6 million clinical cases of malaria are predicted annually given the 10% higher level of outdoor biting observed here. Mosquito species and behavior data together with people’s resting and sleeping patterns are needed to fully measure indoor intervention efficacy and accurately quantify residual transmission.

          Abstract

          The antimalarial efficacy of the most important vector control interventions—long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS)—primarily protect against mosquitoes’ biting people when they are in bed and indoors. Mosquito bites taken outside of these times contribute to residual transmission which determines the maximum effectiveness of current malaria prevention. The likelihood mosquitoes feed outside the time of day when LLINs and IRS can protect people is poorly understood, and the proportion of bites received outdoors may be higher after prolonged vector control. A systematic review of mosquito and human behavior is used to quantify and estimate the public health impact of outdoor biting across Africa. On average 79% of bites by the major malaria vectors occur during the time when people are in bed. This estimate is substantially lower than previous predictions, with results suggesting a nearly 10% lower proportion of bites taken at the time when people are beneath LLINs since the year 2000. Across Africa, this higher outdoor transmission is predicted to result in an estimated 10.6 million additional malaria cases annually if universal LLIN and IRS coverage was achieved. Higher outdoor biting diminishes the cases of malaria averted by vector control. This reduction in LLIN effectiveness appears to be exacerbated in areas where mosquito populations are resistant to insecticides used in bed nets, but no association was found between physiological resistance and outdoor biting. Substantial spatial heterogeneity in mosquito biting behavior between communities could contribute to differences in effectiveness of malaria control across Africa.

          Related collections

          Most cited references46

          • Record: found
          • Abstract: found
          • Article: found
          Is Open Access

          Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania

          Background Insecticide-treated nets (ITNs) and indoor residual spraying (IRS) represent the front-line tools for malaria vector control globally, but are optimally effective where the majority of baseline transmission occurs indoors. In the surveyed area of rural southern Tanzania, bed net use steadily increased over the last decade, reducing malaria transmission intensity by 94%. Methods Starting before bed nets were introduced (1997), and then after two milestones of net use had been reached-75% community-wide use of untreated nets (2004) and then 47% use of ITNs (2009)-hourly biting rates of malaria vectors from the Anopheles gambiae complex and Anopheles funestus group were surveyed. Results In 1997, An. gambiae s.l. and An. funestus mosquitoes exhibited a tendency to bite humans inside houses late at night. For An. gambiae s.l., by 2009, nocturnal activity was less (p = 0.0018). At this time, the sibling species composition of the complex had shifted from predominantly An. gambiae s.s. to predominantly An. arabiensis. For An. funestus, by 2009, nocturnal activity was less (p = 0.0054) as well as the proportion biting indoors (p < 0.0001). At this time, An. funestus s.s. remained the predominant species within this group. As a consequence of these altered feeding patterns, the proportion (mean ± standard error) of human contact with mosquitoes (bites per person per night) occurring indoors dropped from 0.99 ± 0.002 in 1997 to 0.82 ± 0.008 in 2009 for the An. gambiae complex (p = 0.0143) and from 1.00 ± <0.001 to only 0.50 ± 0.048 for the An. funestus complex (p = 0.0004) over the same time period. Conclusions High usage of ITNs can dramatically alter African vector populations so that intense, predominantly indoor transmission is replaced by greatly lowered residual transmission, a greater proportion of which occurs outdoors. Regardless of the underlying mechanism, the residual, self-sustaining transmission will respond poorly to further insecticidal measures within houses. Additional vector control tools which target outdoor biting mosquitoes at the adult or immature stages are required to complement ITNs and IRS.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: found
            Is Open Access

            A new world malaria map: Plasmodium falciparum endemicity in 2010

            Background Transmission intensity affects almost all aspects of malaria epidemiology and the impact of malaria on human populations. Maps of transmission intensity are necessary to identify populations at different levels of risk and to evaluate objectively options for disease control. To remain relevant operationally, such maps must be updated frequently. Following the first global effort to map Plasmodium falciparum malaria endemicity in 2007, this paper describes the generation of a new world map for the year 2010. This analysis is extended to provide the first global estimates of two other metrics of transmission intensity for P. falciparum that underpin contemporary questions in malaria control: the entomological inoculation rate (PfEIR) and the basic reproductive number (PfR). Methods Annual parasite incidence data for 13,449 administrative units in 43 endemic countries were sourced to define the spatial limits of P. falciparum transmission in 2010 and 22,212 P. falciparum parasite rate (PfPR) surveys were used in a model-based geostatistical (MBG) prediction to create a continuous contemporary surface of malaria endemicity within these limits. A suite of transmission models were developed that link PfPR to PfEIR and PfR and these were fitted to field data. These models were combined with the PfPR map to create new global predictions of PfEIR and PfR. All output maps included measured uncertainty. Results An estimated 1.13 and 1.44 billion people worldwide were at risk of unstable and stable P. falciparum malaria, respectively. The majority of the endemic world was predicted with a median PfEIR of less than one and a median PfR c of less than two. Values of either metric exceeding 10 were almost exclusive to Africa. The uncertainty described in both PfEIR and PfR was substantial in regions of intense transmission. Conclusions The year 2010 has a particular significance as an evaluation milestone for malaria global health policy. The maps presented here contribute to a rational basis for control and elimination decisions and can serve as a baseline assessment as the global health community looks ahead to the next series of milestones targeted at 2015.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: found
              Is Open Access

              The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis

              Background This is the second in a series of three articles documenting the geographical distribution of 41 dominant vector species (DVS) of human malaria. The first paper addressed the DVS of the Americas and the third will consider those of the Asian Pacific Region. Here, the DVS of Africa, Europe and the Middle East are discussed. The continent of Africa experiences the bulk of the global malaria burden due in part to the presence of the An. gambiae complex. Anopheles gambiae is one of four DVS within the An. gambiae complex, the others being An. arabiensis and the coastal An. merus and An. melas. There are a further three, highly anthropophilic DVS in Africa, An. funestus, An. moucheti and An. nili. Conversely, across Europe and the Middle East, malaria transmission is low and frequently absent, despite the presence of six DVS. To help control malaria in Africa and the Middle East, or to identify the risk of its re-emergence in Europe, the contemporary distribution and bionomics of the relevant DVS are needed. Results A contemporary database of occurrence data, compiled from the formal literature and other relevant resources, resulted in the collation of information for seven DVS from 44 countries in Africa containing 4234 geo-referenced, independent sites. In Europe and the Middle East, six DVS were identified from 2784 geo-referenced sites across 49 countries. These occurrence data were combined with expert opinion ranges and a suite of environmental and climatic variables of relevance to anopheline ecology to produce predictive distribution maps using the Boosted Regression Tree (BRT) method. Conclusions The predicted geographic extent for the following DVS (or species/suspected species complex*) is provided for Africa: Anopheles (Cellia) arabiensis, An. (Cel.) funestus*, An. (Cel.) gambiae, An. (Cel.) melas, An. (Cel.) merus, An. (Cel.) moucheti and An. (Cel.) nili*, and in the European and Middle Eastern Region: An. (Anopheles) atroparvus, An. (Ano.) labranchiae, An. (Ano.) messeae, An. (Ano.) sacharovi, An. (Cel.) sergentii and An. (Cel.) superpictus*. These maps are presented alongside a bionomics summary for each species relevant to its control.
                Bookmark

                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                23 July 2019
                8 July 2019
                8 July 2019
                : 116
                : 30
                : 15086-15095
                Affiliations
                [1] aMRC Centre for Global Infectious Disease Analysis, Department of Infectious Disease Epidemiology, Imperial College London, W2 1PG London, United Kingdom;
                [2] bFaculty of Health and Medical Sciences, University of Surrey, GU2 7XH Guildford, United Kingdom;
                [3] cMRC Laboratory of Molecular Biology, University of Cambridge, CB2 0QH Cambridge, United Kingdom;
                [4] dUS President’s Malaria Initiative, US Agency for International Development, Washington, DC 20004;
                [5] eEnvironmental Health and Ecological Sciences, Ifakara Health Institute, Bagamoyo, Tanzania;
                [6] fHealth Interventions Unit, Department of Epidemiology and Public Health, Swiss Institute of Tropical and Public Health, 4002 Basel, Switzerland;
                [7] gUniversity of Basel, 4003 Basel, Switzerland;
                [8] hNational Malaria Control Program, Ministry of Health, Asmara, State of Eritrea;
                [9] iUniversity of Asmara, State of Eritrea;
                [10] jSchool of Mathematical Sciences, Queen Mary University of London, E1 4NS London, United Kingdom
                Author notes
                1To whom correspondence may be addressed. Email: e.sherrard-smith@ 123456imperial.ac.uk .

                Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved June 12, 2019 (received for review December 5, 2018)

                Author contributions: E.S.-S., J.T.G., and T.S.C. designed research; E.S.-S. and J.E.S. performed research; A.D.B., C.F., L.C.N., S.J.M., S.M., J.D.C., and S.B. contributed new reagents/analytic tools; E.S.-S., J.E.S., S.B., P.W., and T.S.C. analyzed data; and E.S.-S. and T.S.C. wrote the paper.

                Author information
                http://orcid.org/0000-0001-8317-7992
                Article
                201820646
                10.1073/pnas.1820646116
                6660788
                31285346
                58ffba47-68e3-49a7-b323-d8ef554b596b
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

                History
                Page count
                Pages: 10
                Funding
                Funded by: Innovative Vector Control Consortium (IVCC)
                Award ID: P76200
                Award Recipient : Ellie Sherrard-Smith Award Recipient : Thomas S Churcher
                Funded by: Wellcome Trust
                Award ID: 200222/Z/15/Z
                Award Recipient : Ellie Sherrard-Smith Award Recipient : Thomas S Churcher
                Funded by: MiRA and the UK Medical Research Council (MRC) / UK Department for International Development (DFID)
                Award ID: MRC/DFID Concordat agreement
                Award Recipient : Ellie Sherrard-Smith Award Recipient : Thomas S Churcher
                Categories
                PNAS Plus
                Biological Sciences
                Ecology
                PNAS Plus

                plasmodium falciparum,malaria transmission,llin efficacy,vector interventions,anopheles

                Comments

                Comment on this article