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      Rethinking the extrinsic incubation period of malaria parasites

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          Abstract

          The time it takes for malaria parasites to develop within a mosquito, and become transmissible, is known as the extrinsic incubation period, or EIP. EIP is a key parameter influencing transmission intensity as it combines with mosquito mortality rate and competence to determine the number of mosquitoes that ultimately become infectious. In spite of its epidemiological significance, data on EIP are scant. Current approaches to estimate EIP are largely based on temperature-dependent models developed from data collected on parasite development within a single mosquito species in the 1930s. These models assume that the only factor affecting EIP is mean environmental temperature. Here, we review evidence to suggest that in addition to mean temperature, EIP is likely influenced by genetic diversity of the vector, diversity of the parasite, and variation in a range of biotic and abiotic factors that affect mosquito condition. We further demonstrate that the classic approach of measuring EIP as the time at which mosquitoes first become infectious likely misrepresents EIP for a mosquito population. We argue for a better understanding of EIP to improve models of transmission, refine predictions of the possible impacts of climate change, and determine the potential evolutionary responses of malaria parasites to current and future mosquito control tools.

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          The online version of this article (10.1186/s13071-018-2761-4) contains supplementary material, which is available to authorized users.

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          Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti.

          Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vector-pathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20 °C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10 °C) or constant temperature. A thermodynamic model predicted that at mean temperatures 18 °C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.
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            Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing

            Malaria elimination strategies require surveillance of the parasite population for genetic changes that demand a public health response, such as new forms of drug resistance. 1,2 Here we describe methods for large-scale analysis of genetic variation in Plasmodium falciparum by deep sequencing of parasite DNA obtained from the blood of patients with malaria, either directly or after short term culture. Analysis of 86,158 exonic SNPs that passed genotyping quality control in 227 samples from Africa, Asia and Oceania provides genome-wide estimates of allele frequency distribution, population structure and linkage disequilibrium. By comparing the genetic diversity of individual infections with that of the local parasite population, we derive a metric of within-host diversity that is related to the level of inbreeding in the population. An open-access web application has been established for exploration of regional differences in allele frequency and of highly differentiated loci in the P. falciparum genome.
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              Two Chikungunya Isolates from the Outbreak of La Reunion (Indian Ocean) Exhibit Different Patterns of Infection in the Mosquito, Aedes albopictus

              Background A Chikungunya (CHIK) outbreak hit La Réunion Island in 2005–2006. The implicated vector was Aedes albopictus. Here, we present the first study on the susceptibility of Ae. albopictus populations to sympatric CHIKV isolates from La Réunion Island and compare it to other virus/vector combinations. Methodology and Findings We orally infected 8 Ae. albopictus collections from La Réunion and 3 from Mayotte collected in March 2006 with two Chikungunya virus (CHIKV) from La Réunion: (i) strain 05.115 collected in June 2005 with an Alanine at the position 226 of the glycoprotein E1 and (ii) strain 06.21 collected in November 2005 with a substitution A226V. Two other CHIKV isolates and four additional mosquito strains/species were also tested. The viral titer of the infectious blood-meal was 107 plaque forming units (pfu)/mL. Dissemination rates were assessed by immunofluorescent staining on head squashes of surviving females 14 days after infection. Rates were at least two times higher with CHIKV 06.21 compared to CHIKV 05.115. In addition, 10 individuals were analyzed every day by quantitative RT-PCR. Viral RNA was quantified on (i) whole females and (ii) midguts and salivary glands of infected females. When comparing profiles, CHIKV 06.21 produced nearly 2 log more viral RNA copies than CHIKV 05.115. Furthermore, females infected with CHIKV 05.115 could be divided in two categories: weakly susceptible or strongly susceptible, comparable to those infected by CHIKV 06.21. Histological analysis detected the presence of CHIKV in salivary glands two days after infection. In addition, Ae. albopictus from La Réunion was as efficient vector as Ae. aegypti and Ae. albopictus from Vietnam when infected with the CHIKV 06.21. Conclusions Our findings support the hypothesis that the CHIK outbreak in La Réunion Island was due to a highly competent vector Ae. albopictus which allowed an efficient replication and dissemination of CHIKV 06.21.
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                Author and article information

                Contributors
                jo.ohm@psu.edu
                Francesco.Baldini@glasgow.ac.uk
                pub76@psu.edu
                thierry.lefevre@ird.fr
                pennymath@lynch-fm.demon.co.uk
                eus57@psu.edu
                saw359@psu.edu
                mbt13@psu.edu
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                12 March 2018
                12 March 2018
                2018
                : 11
                : 178
                Affiliations
                [1 ]ISNI 0000 0001 2097 4281, GRID grid.29857.31, Center for Infectious Disease Dynamics, , Pennsylvania State University, ; University Park, PA USA
                [2 ]ISNI 0000 0001 2193 314X, GRID grid.8756.c, Institute of Biodiversity Animal Health and Comparative Medicine, , University of Glasgow, ; Glasgow, Scotland UK
                [3 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, MIVEGEC, IRD, CNRS, , University of Montpellier, ; Montpellier, France
                [4 ]ISNI 0000 0004 1936 8024, GRID grid.8391.3, College of Life and Environmental Sciences, Penryn Campus, , University of Exeter, ; Cornwall, UK
                Article
                2761
                10.1186/s13071-018-2761-4
                5848458
                29530073
                d3e655b7-5463-4027-9539-4860b885f98d
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 18 December 2017
                : 28 February 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000060, NIH NIAID;
                Award ID: R01AI110793
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000155, Division of Environmental Biology;
                Award ID: 1518681
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003043, EMBO;
                Award ID: 43-2014
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001961, AXA Research Fund;
                Award ID: 14-AXA-PDOC-130
                Award Recipient :
                Funded by: ANR
                Award ID: ANR grant 16-CE35-0007
                Award Recipient :
                Categories
                Review
                Custom metadata
                © The Author(s) 2018

                Parasitology
                malaria,mosquito,extrinsic incubation period,eip,temperature
                Parasitology
                malaria, mosquito, extrinsic incubation period, eip, temperature

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