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      Vector competence of Italian Aedes albopictus populations for the chikungunya virus (E1-226V)

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          Abstract

          Background

          Chikungunya virus (CHIKV) is an emerging arbovirus, belonging to the Togaviridae family, Alphavirus genus, transmitted by Aedes spp. mosquitoes. Since 2007, two different CHIKV strains (E1-226A and E1-226V) have been responsible for outbreaks in European countries, including Italy, sustained by Ae. albopictus mosquitoes.

          Findings

          In this study, we assessed the susceptibility to the CHIKV E1-226V, strain responsible for the Italian 2007 outbreak, of eight Ae. albopictus populations collected in Northern, Central, Southern, and Island Italy, by experimental infections. Vector competence was evaluated by estimating infection, dissemination, and transmission rates (IR, DR, TR), through detection of the virus in the bodies, legs plus wings, and saliva, respectively. Additionally, vertical transmission was evaluated by the detection of the virus in the offspring. The results of our study demonstrated that the Italian populations of Ae. albopictus tested were susceptible to CHIKV infection, and can disseminate the virus outside the midgut barrier with high values of IR and DR. Viral infectious RNA was detected in the saliva of three populations from Central, Southern, and Island Italy, also tested for TR and population transmission rate (PTR) values. No progeny of the first and second gonotrophic cycle were positive for CHIKV.

          Conclusions

          This study strongly confirms the role of Ae. albopictus as a potential CHIKV vector in Italy. This may represent a threat, especially considering both the high density of this species, which is widespread throughout the country, and the increasing number of cases of imported arboviruses.

          Author summary

          Aedes albopictus is a proven vector of more than 20 different arboviruses and, as demonstrated by experimental infections, is an efficient vector of chikungunya virus (CHIKV) in several countries. In Italy this widespread species caused the first outbreak of CHIKV in Europe in 2007 (Emilia-Romagna region) and recently, after 10 years, two different outbreaks in the Central and Southern part of the country (Latium and Calabria regions) were reported. Symptoms of CHIKV are arthralgia and joint pain, skin rash, primarily of the trunk and limbs, but also commonly fever and myalgia. Complications of this disease are rare, but long-term sequelae often occur in a considerable number of patients in particular, in children, the elderly, and patients with chronic diseases. The recent circulation of CHIKV in Italy has highlighted the importance of investigating vector competence of Italian populations of Ae. albopictus from different areas. In this study, we experimentally infected several mosquito populations in order to assess the real risk of CHIKV epidemics in temperate zones and support efficient surveillance and control strategies.

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          Most cited references36

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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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            An extension of the Wilcoxon rank-sum test is developed to handle the situation in which a variable is measured for individuals in three or more (ordered) groups and a non-parametric test for trend across these groups is desired. The uses of the test are illustrated by two examples from cancer research.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Methodology
                Role: Methodology
                Role: Methodology
                Role: Methodology
                Role: Methodology
                Role: Data curationRole: Formal analysis
                Role: Supervision
                Role: Supervision
                Role: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: 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
                19 April 2018
                April 2018
                : 12
                : 4
                : e0006435
                Affiliations
                [1 ] Unit of Vector-borne Diseases DMI Department, Istituto Superiore di Sanità, Rome, Italy
                [2 ] Unit of Arbo, Hanta and Emerging Viruses, DMI Department, Istituto Superiore di Sanità, Rome, Italy
                [3 ] Technical Scientific Statistics Service of the Italian National Institute of Health, Istituto Superiore di Sanità, Rome, Italy
                INDEPENDENT RESEARCHER, UNITED STATES
                Author notes

                The authors declare that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-0179-5277
                Article
                PNTD-D-17-02044
                10.1371/journal.pntd.0006435
                5929569
                29672511
                46948d30-60b4-4383-bfdc-203ac6fb7868
                © 2018 Severini 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
                : 20 December 2017
                : 8 April 2018
                Page count
                Figures: 2, Tables: 1, Pages: 14
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
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                Mosquitoes
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                Species Interactions
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                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
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                Arthropoda
                Insects
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                Anatomy
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                Custom metadata
                vor-update-to-uncorrected-proof
                2018-05-01
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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