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Armstrong JF. Neurologic Assessment and Critical Care of Exotic Animals: Approach to the Neurologic Exam, Species Differences, Prognostic Scales, Commonly Encountered Conditions, Ancillary Diagnostic Tests, and Caring for Neurologically Impaired Patients. Vet Clin North Am Exot Anim Pract 2023:S1094-9194(23)00025-7. [PMID: 37385906 DOI: 10.1016/j.cvex.2023.05.007] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 07/01/2023]
Abstract
Many disorders of other body systems have been well characterized in exotic species; however, data regarding neurologic conditions is limited. Across some of these species, correlates between feline and canine neurology can be made, but variations in the nervous system anatomy make evaluation more challenging. With accurate neurolocalization a focused list of differential diagnoses can be created. Performing the neurologic examination should be methodical for all patients, and the order and extent of examination may depend upon the patient's clinical condition and cooperation. Applications of objective scale measures (such as coma scales), and ancillary diagnostics (electrodiagnostics, advanced imaging, biopsy techniques, and BAER testing) complement physical assessment and clinicopathologic assessment in these neurologic patients. Once a neurolocalization, likely diagnosis, and prognosis have been established, specific considerations for hospitalization and care of neurologic patients can be implemented while treatment is instituted.
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Albayrak H, Sahindokuyucu I, Muftuoglu B, Tamer C, Kadi H, Ozan E, Yilmaz O, Kilic H, Kurucay HN, Coven F, Gumusova S, Yazici Z, Elhag AE. Sentinel serosurveillance of backyard hens proved West Nile virus circulation in the western provinces of Turkey. Vet Med Sci 2021; 7:2348-2352. [PMID: 34323396 PMCID: PMC8604147 DOI: 10.1002/vms3.589] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022] Open
Abstract
West Nile virus (WNV) is a mosquito-borne virus of a re-emergence importance with a wide range of vertebrate hosts. Granted, it causes asymptomatic infection, but fatal cases and neurologic disorders were also recorded, especially in humans, horses and some exposed birds. The virus is globally spread and birds are considered an amplifying and reservoir host of WNV, helping to spread the disease due to their close contact with main hosts. In this study, we aimed to detect the presence of antibodies against WNV in backyard hens that were reared in the western Anatolian part of Turkey. A total of 480 chicken sera were randomly collected from six provinces in the west of Turkey (Mugla, Izmir, Aydin, Afyonkarahisar, Kutahya and Manisa) with 80 samples from each province (40 in spring and 40 in fall seasons). They were tested by using a competitive ELISA method to identify the specific avian antibodies of IgG that produced against the WNV envelope proteins (pr-E). Twelve of 480 (2.5%) sera were found seropositive, three of these positive sera were detected from the Izmir province (3.75%) collected in the spring session and the other nine positive sera were detected from the Mugla province (11.25%) collected in the fall session. Both of these provinces are located seaside and have suitable climate conditions for vectors of infection. The results indicated that WNV infection is in circulation in these provinces, and that may put the other susceptible vertebrates under risk of infection.
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Affiliation(s)
- Harun Albayrak
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Ismail Sahindokuyucu
- Bornova Veterinary Control Institute, Ministry of Agriculture and Forestry, Izmir, Turkey
| | - Bahadir Muftuoglu
- Department of Experimental Animals, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Cuneyt Tamer
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Hamza Kadi
- Samsun Veterinary Control Institute, Ministry of Agriculture and Forestry, Samsun, Turkey
| | - Emre Ozan
- Department of Experimental Animals, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Ozge Yilmaz
- Bornova Veterinary Control Institute, Ministry of Agriculture and Forestry, Izmir, Turkey
| | - Hamza Kilic
- Bornova Veterinary Control Institute, Ministry of Agriculture and Forestry, Izmir, Turkey
| | - Hanne Nur Kurucay
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Fethiye Coven
- Bornova Veterinary Control Institute, Ministry of Agriculture and Forestry, Izmir, Turkey
| | - Semra Gumusova
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Zafer Yazici
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey
| | - Ahmed Eisa Elhag
- Department of Virology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey.,Department of Preventive Medicine and Clinical Studies, Faculty of Veterinary Sciences, University of Gadarif, Al Qadarif, Sudan
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Jiménez de Oya N, Escribano-Romero E, Blázquez AB, Martín-Acebes MA, Saiz JC. Current Progress of Avian Vaccines Against West Nile Virus. Vaccines (Basel) 2019; 7:vaccines7040126. [PMID: 31547632 PMCID: PMC6963603 DOI: 10.3390/vaccines7040126] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/31/2019] [Revised: 09/19/2019] [Accepted: 09/19/2019] [Indexed: 01/15/2023] Open
Abstract
Birds are the main natural host of West Nile virus (WNV), the worldwide most distributed mosquito-borne flavivirus, but humans and equids can also be sporadic hosts. Many avian species have been reported as susceptible to WNV, particularly corvids. In the case that clinical disease develops in birds, this is due to virus invasion of different organs: liver, spleen, kidney, heart, and mainly the central nervous system, which can lead to death 24–48 h later. Nowadays, vaccines have only been licensed for use in equids; thus, the availability of avian vaccines would benefit bird populations, both domestic and wild ones. Such vaccines could be used in endangered species housed in rehabilitation and wildlife reserves, and in animals located at zoos and other recreational installations, but also in farm birds, and in those that are grown for hunting and restocking activities. Even more, controlling WNV infection in birds can also be useful to prevent its spread and limit outbreaks. So far, different commercial and experimental vaccines (inactivated, attenuated, and recombinant viruses, and subunits and DNA-based candidates) have been evaluated, with various regimens, both in domestic and wild avian species. However, there are still disadvantages that must be overcome before avian vaccination can be implemented, such as its cost-effectiveness for domestic birds since in many species the pathogenicity is low or zero, or the viability of being able to achieve collective immunity in wild birds in freedom. Here, a comprehensive review of what has been done until now in the field of avian vaccines against WNV is presented and discussed.
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Affiliation(s)
- Nereida Jiménez de Oya
- Department of Biotechnology, National Agricultural and Food Research and Technology Institute (INIA), 28040 Madrid, Spain.
| | - Estela Escribano-Romero
- Department of Biotechnology, National Agricultural and Food Research and Technology Institute (INIA), 28040 Madrid, Spain.
| | - Ana-Belén Blázquez
- Department of Biotechnology, National Agricultural and Food Research and Technology Institute (INIA), 28040 Madrid, Spain.
| | - Miguel A Martín-Acebes
- Department of Biotechnology, National Agricultural and Food Research and Technology Institute (INIA), 28040 Madrid, Spain.
| | - Juan-Carlos Saiz
- Department of Biotechnology, National Agricultural and Food Research and Technology Institute (INIA), 28040 Madrid, Spain.
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Jiménez de Oya N, Escribano-Romero E, Camacho MC, Blazquez AB, Martín-Acebes MA, Höfle U, Saiz JC. A Recombinant Subviral Particle-Based Vaccine Protects Magpie ( Pica pica) Against West Nile Virus Infection. Front Microbiol 2019; 10:1133. [PMID: 31231320 PMCID: PMC6560071 DOI: 10.3389/fmicb.2019.01133] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/15/2019] [Accepted: 05/03/2019] [Indexed: 01/19/2023] Open
Abstract
The mosquito-borne West Nile virus (WNV) is a highly neurovirulent Flavivirus currently representing an emergent zoonotic concern. WNV cycles in nature between mosquito vectors and birds that act as amplifier hosts and play an essential role in virus ecology, being, thus, WNV a threat to many species. Availability of an efficient avian vaccine would benefit certain avian populations, both birds grown for hunting and restocking activities, as well as endangered species in captive breeding projects, wildlife reservations, and recreation installations, and would be useful to prevent and contain outbreaks. Avian vaccination would be also of interest to limit WNV spillover to humans or horses from susceptible bird species that live in urbanized landscapes, like magpies. Herein, we have addressed the efficacy of a single dose of a WNV recombinant subviral particle (RSP) vaccine in susceptible magpie (Pica pica). The protective capacity of the RSP-based vaccine was demonstrated upon challenge of magpies with 5 × 103 plaque forming units of a neurovirulent WNV strain. A significant improvement in survival rates of immunized birds was recorded when compared to vehicle-inoculated animals (71.4 vs. 22.2%, respectively). Viremia, which is directly related to the capacity of a host to be competent for virus transmission, was reduced in vaccinated animals, as was the presence of infectious virus in feather follicles. Bird-to-bird transmission was recorded in three of six unchallenged (contact) magpies housed with non-vaccinated WNV-infected birds, but not in contact animals housed with vaccinated WNV-infected magpies. These results demonstrate the protective efficacy of the RSP-based vaccine in susceptible birds against WNV infection and its value in controlling the spread of the virus.
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Affiliation(s)
- Nereida Jiménez de Oya
- Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain
| | - Estela Escribano-Romero
- Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain
| | - María-Cruz Camacho
- Grupo de Sanidad y Biotecnología SaBio, Instituto de Investigación en Recursos Cinegéticos IREC, CSIC-UCLM-JCCM, Ciudad Real, Spain
| | - Ana-Belén Blazquez
- Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain
| | - Miguel A Martín-Acebes
- Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain
| | - Ursula Höfle
- Grupo de Sanidad y Biotecnología SaBio, Instituto de Investigación en Recursos Cinegéticos IREC, CSIC-UCLM-JCCM, Ciudad Real, Spain
| | - Juan-Carlos Saiz
- Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain
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Benzarti E, Linden A, Desmecht D, Garigliany M. Mosquito-borne epornitic flaviviruses: an update and review. J Gen Virol 2019; 100:119-132. [PMID: 30628886 DOI: 10.1099/jgv.0.001203] [Citation(s) in RCA: 52] [Impact Index Per Article: 8.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022] Open
Abstract
West Nile Virus, Usutu virus, Bagaza virus, Israel turkey encephalitis virus and Tembusu virus currently constitute the five flaviviruses transmitted by mosquito bites with a marked pathogenicity for birds. They have been identified as the causative agents of severe neurological symptoms, drop in egg production and/or mortalities among avian hosts. They have also recently shown an expansion of their geographic distribution and/or a rise in cases of human infection. This paper is the first up-to-date review of the pathology of these flaviviruses in birds, with a special emphasis on the difference in susceptibility among avian species, in order to understand the specificity of the host spectrum of each of these viruses. Furthermore, given the lack of a clear prophylactic approach against these viruses in birds, a meta-analysis of vaccination trials conducted to date on these animals is given to constitute a solid platform from which designing future studies.
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Affiliation(s)
- Emna Benzarti
- 1FARAH Research Center, Department of Pathology, Faculty of Veterinary Medicine, University of Liège, Sart Tilman B43, B-4000 Liège, Belgium
| | - Annick Linden
- 2FARAH Research Center, Surveillance Network for Wildlife Diseases, Faculty of Veterinary Medicine, University of Liège, Sart Tilman B43, B-4000 Liège, Belgium
| | - Daniel Desmecht
- 1FARAH Research Center, Department of Pathology, Faculty of Veterinary Medicine, University of Liège, Sart Tilman B43, B-4000 Liège, Belgium
| | - Mutien Garigliany
- 1FARAH Research Center, Department of Pathology, Faculty of Veterinary Medicine, University of Liège, Sart Tilman B43, B-4000 Liège, Belgium
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Emerging Mosquito-Borne Threats and the Response from European and Eastern Mediterranean Countries. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2018; 15:ijerph15122775. [PMID: 30544521 PMCID: PMC6313739 DOI: 10.3390/ijerph15122775] [Citation(s) in RCA: 30] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/30/2018] [Revised: 11/22/2018] [Accepted: 12/04/2018] [Indexed: 12/15/2022]
Abstract
Mosquito-borne viruses are the cause of some of the greatest burdens to human health worldwide, particularly in tropical regions where both human populations and mosquito numbers are abundant. Due to a combination of anthropogenic change, including the effects on global climate and wildlife migration there is strong evidence that temperate regions are undergoing repeated introduction of mosquito-borne viruses and the re-emergence of viruses that previously were not detected by surveillance. In Europe, the repeated introductions of West Nile and Usutu viruses have been associated with bird migration from Africa, whereas the autochthonous transmission of chikungunya and dengue viruses has been driven by a combination of invasive mosquitoes and rapid transcontinental travel by infected humans. In addition to an increasing number of humans at risk, livestock and wildlife, are also at risk of infection and disease. This in turn can affect international trade and species diversity, respectively. Addressing these challenges requires a range of responses both at national and international level. Increasing the understanding of mosquito-borne transmission of viruses and the development of rapid detection methods and appropriate therapeutics (vaccines / antivirals) all form part of this response. The aim of this review is to consider the range of mosquito-borne viruses that threaten public health in Europe and the eastern Mediterranean, and the national response of a number of countries facing different levels of threat.
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Zhang L, Li Z, Zhang Q, Sun M, Li S, Su W, Hu X, He W, Su J. Efficacy assessment of an inactivated Tembusu virus vaccine candidate in ducks. Res Vet Sci 2017; 110:72-78. [DOI: 10.1016/j.rvsc.2016.11.002] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2016] [Revised: 10/28/2016] [Accepted: 11/01/2016] [Indexed: 10/20/2022]
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Lustig Y, Hindiyeh M, Orshan L, Weiss L, Koren R, Katz-Likvornik S, Zadka H, Glatman-Freedman A, Mendelson E, Shulman LM. Mosquito Surveillance for 15 Years Reveals High Genetic Diversity Among West Nile Viruses in Israel. J Infect Dis 2015; 213:1107-14. [PMID: 26597260 DOI: 10.1093/infdis/jiv556] [Citation(s) in RCA: 27] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/06/2015] [Accepted: 11/12/2015] [Indexed: 12/16/2022] Open
Abstract
West Nile Virus (WNV) is endemic in Israel and has been the cause of several outbreaks in recent years. In 2000, a countrywide mosquito survey was established to monitor WNV activity and characterize viral genotypes in Israel. We analyzed data from 7135 pools containing 277 186 mosquitoes collected over the past 15 years and, here, report partial sequences of WNV genomes obtained from 102 of the 336 positive mosquito pools. Phylogenetic analysis demonstrated that cluster 4 and the Mediterranean and Eastern European subtypes of cluster 2 within WNV lineage 1 circulated in Israel, as did WNV lineage 2, highlighting a high genetic diversity of WNV genotypes in our region. As a major crossroads for bird migration between Africa and Eurasia and with a long history of human infection, Israel serves as a resource hub for WNV in Africa and Eurasia and provides valuable information on WNV circulation in these regions.
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Affiliation(s)
- Yaniv Lustig
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer
| | - Musa Hindiyeh
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer Department of Epidemiology and Preventive Medicine, School of Public Health, Sackler Faculty of Medicine, Tel-Aviv University, Israel
| | - Laor Orshan
- Laboratory of Entomology, Ministry of Health, Jerusalem
| | - Leah Weiss
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer
| | - Ravit Koren
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer
| | - Shiri Katz-Likvornik
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer
| | - Hila Zadka
- Israel Center for Disease Control, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer
| | - Aharona Glatman-Freedman
- Israel Center for Disease Control, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer New York Medical College, Valhalla, New York
| | - Ella Mendelson
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer Department of Epidemiology and Preventive Medicine, School of Public Health, Sackler Faculty of Medicine, Tel-Aviv University, Israel
| | - Lester M Shulman
- Central Virology Laboratory, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer Department of Epidemiology and Preventive Medicine, School of Public Health, Sackler Faculty of Medicine, Tel-Aviv University, Israel
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A review of vaccine approaches for West Nile virus. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2013; 10:4200-23. [PMID: 24025396 PMCID: PMC3799512 DOI: 10.3390/ijerph10094200] [Citation(s) in RCA: 33] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 07/08/2013] [Revised: 09/02/2013] [Accepted: 09/05/2013] [Indexed: 01/19/2023]
Abstract
The West Nile virus (WNC) first appeared in North America in 1999. The North American lineages of WNV were characterized by the presence of neuroinvasive and neurovirulent strains causing disease and death in humans, birds and horses. The 2012 WNV season in the United States saw a massive spike in the number of neuroinvasive cases and deaths similar to what was seen in the 2002–2003 season, according to the West Nile virus disease cases and deaths reported to the CDC by year and clinical presentation, 1999–2012, by ArboNET (Arboviral Diseases Branch, Centers for Disease Control and Prevention). In addition, the establishment and recent spread of lineage II WNV virus strains into Western Europe and the presence of neurovirulent and neuroinvasive strains among them is a cause of major concern. This review discusses the advances in the development of vaccines and biologicals to combat human and veterinary West Nile disease.
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Martín-Acebes MA, Saiz JC. West Nile virus: A re-emerging pathogen revisited. World J Virol 2012; 1:51-70. [PMID: 24175211 PMCID: PMC3782267 DOI: 10.5501/wjv.v1.i2.51] [Citation(s) in RCA: 65] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/19/2011] [Revised: 02/16/2012] [Accepted: 03/05/2012] [Indexed: 02/05/2023] Open
Abstract
West Nile virus (WNV), a flavivirus of the Flaviviridae family, is maintained in nature in an enzootic transmission cycle between avian hosts and ornithophilic mosquito vectors, although the virus occasionally infects other vertebrates. WNV causes sporadic disease outbreaks in horses and humans, which may result in febrile illness, meningitis, encephalitis and flaccid paralysis. Until recently, its medical and veterinary health concern was relatively low; however, the number, frequency and severity of outbreaks with neurological consequences in humans and horses have lately increased in Europe and the Mediterranean basin. Since its introduction in the Americas, the virus spread across the continent with worrisome consequences in bird mortality and a considerable number of outbreaks among humans and horses, which have resulted in the largest epidemics of neuroinvasive WNV disease ever documented. Surprisingly, its incidence in human and animal health is very different in Central and South America, and the reasons for it are not yet understood. Even though great advances have been obtained lately regarding WNV infection, and although efficient equine vaccines are available, no specific treatments or vaccines for human use are on the market. This review updates the most recent investigations in different aspects of WNV life cycle: molecular virology, transmission dynamics, host range, clinical presentations, epidemiology, ecology, diagnosis, control, and prevention, and highlights some aspects that certainly require further research.
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Affiliation(s)
- Miguel A Martín-Acebes
- Miguel A Martín-Acebes, Juan-Carlos Saiz, Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, 28040 Madrid, Spain
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Sun E, Zhao J, Liu N, Yang T, Xu Q, Qin Y, Bu Z, Yang Y, Lunt RA, Wang L, Wu D. Comprehensive mapping of common immunodominant epitopes in the West Nile virus nonstructural protein 1 recognized by avian antibody responses. PLoS One 2012; 7:e31434. [PMID: 22347477 PMCID: PMC3276514 DOI: 10.1371/journal.pone.0031434] [Citation(s) in RCA: 12] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2011] [Accepted: 01/07/2012] [Indexed: 11/19/2022] Open
Abstract
West Nile virus (WNV) is a mosquito-borne flavivirus that primarily infects birds but occasionally infects humans and horses. Certain species of birds, including crows, house sparrows, geese, blue jays and ravens, are considered highly susceptible hosts to WNV. The nonstructural protein 1 (NS1) of WNV can elicit protective immune responses, including NS1-reactive antibodies, during infection of animals. The antigenicity of NS1 suggests that NS1-reactive antibodies could provide a basis for serological diagnostic reagents. To further define serological reagents for diagnostic use, the antigenic sites in NS1 that are targeted by host immune responses need to be identified and the potential diagnostic value of individual antigenic sites also needs to be defined. The present study describes comprehensive mapping of common immunodominant linear B-cell epitopes in the WNV NS1 using avian WNV NS1 antisera. We screened antisera from chickens, ducks and geese immunized with purified NS1 for reactivity against 35 partially overlapping peptides covering the entire WNV NS1. This study identified twelve, nine and six peptide epitopes recognized by chicken, duck and goose antibody responses, respectively. Three epitopes (NS1-3, 14 and 24) were recognized by antibodies elicited by immunization in all three avian species tested. We also found that NS1-3 and 24 were WNV-specific epitopes, whereas the NS1-14 epitope was conserved among the Japanese encephalitis virus (JEV) serocomplex viruses based on the reactivity of avian WNV NS1 antisera against polypeptides derived from the NS1 sequences of viruses of the JEV serocomplex. Further analysis showed that the three common polypeptide epitopes were not recognized by antibodies in Avian Influenza Virus (AIV), Newcastle Disease Virus (NDV), Duck Plague Virus (DPV) and Goose Parvovirus (GPV) antisera. The knowledge and reagents generated in this study have potential applications in differential diagnostic approaches and subunit vaccines development for WNV and other viruses of the JEV serocomplex.
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Affiliation(s)
- Encheng Sun
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
- Graduate School of Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China
| | - Jing Zhao
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
- Graduate School of Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China
| | - Nihong Liu
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
| | - Tao Yang
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
| | - Qingyuan Xu
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
| | - Yongli Qin
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
- Graduate School of Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China
| | - Zhigao Bu
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
| | - Yinhui Yang
- Beijing Institute of Microbiology and Epidemiology, Beijing, People's Republic of China
| | - Ross A. Lunt
- Australian Animal Health Laboratory, CSIRO Livestock Industries, Geelong, Australia
| | - Linfa Wang
- Australian Animal Health Laboratory, CSIRO Livestock Industries, Geelong, Australia
| | - Donglai Wu
- The Key Laboratory of Veterinary Public Health, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China
- * E-mail:
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12
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Beasley DWC. Vaccines and immunotherapeutics for the prevention and treatment of infections with West Nile virus. Immunotherapy 2011; 3:269-85. [PMID: 21322763 DOI: 10.2217/imt.10.93] [Citation(s) in RCA: 56] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/16/2022] Open
Abstract
The emergence of West Nile virus (WNV) in North America in 1999 as a cause of severe neurological disease in humans, horses and birds stimulated development of vaccines for human and veterinary use, as well as polyclonal/monoclonal antibodies and other immunomodulating compounds for use as therapeutics. Although disease incidence in North America has declined since the peak epidemics in 2002-2003, the virus has continued to be annually transmitted in the Americas and to cause periodic epidemics in Europe and the Middle East. Continued transmission of the virus with human and animal disease suggests that vaccines and therapeutics for the prevention and treatment of WNV disease could be of great benefit. This article focuses on progress in development and evaluation of vaccines and immunotherapeutics for the prevention and treatment of WNV disease in humans and animals.
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Affiliation(s)
- David W C Beasley
- Department of Microbiology & Immunology, Sealy Center for Vaccine Development, Center for Biodefense & Emerging Infectious Diseases, Institute for Human Infections & Immunity, & Galveston National Laboratory, The University of Texas Medical Branch, Galveston, TX 77555-0609, USA.
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13
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Brault AC. Changing patterns of West Nile virus transmission: altered vector competence and host susceptibility. Vet Res 2009; 40:43. [PMID: 19406093 PMCID: PMC2695027 DOI: 10.1051/vetres/2009026] [Citation(s) in RCA: 79] [Impact Index Per Article: 4.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/04/2009] [Accepted: 04/29/2009] [Indexed: 12/11/2022] Open
Abstract
West Nile virus (WNV) is a flavivirus (Flaviviridae) transmitted between Culex spp. mosquitoes and avian hosts. The virus has dramatically expanded its geographic range in the past ten years. Increases in global commerce, climate change, ecological factors and the emergence of novel viral genotypes likely play significant roles in the emergence of this virus; however, the exact mechanism and relative importance of each is uncertain. Previously WNV was primarily associated with febrile illness of children in endemic areas, but it was identified as a cause of neurological disease in humans in 1994. This modulation in disease presentation could be the result of the emergence of a more virulent genotype as well as the progression of the virus into areas in which the age structure of immunologically naïve individuals makes them more susceptible to severe neurological disease. Since its introduction to North America in 1999, a novel WNV genotype has been identified that has been demonstrated to disseminate more rapidly and with greater efficiency at elevated temperatures than the originally introduced strain, indicating the potential importance of temperature as a selective criteria for the emergence of WNV genotypes with increased vectorial capacity. Even prior to the North American introduction, a mutation associated with increased replication in avian hosts, identified to be under adaptive evolutionary pressure, has been identified, indicating that adaptation for increased replication within vertebrate hosts could play a role in increased transmission efficiency. Although stable in its evolutionary structure, WNV has demonstrated the capacity for rapidly adapting to both vertebrate hosts and invertebrate vectors and will likely continue to exploit novel ecological niches as it adapts to novel transmission foci.
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Affiliation(s)
- Aaron C Brault
- Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
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14
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Shrestha B, Ng T, Chu HJ, Noll M, Diamond MS. The relative contribution of antibody and CD8+ T cells to vaccine immunity against West Nile encephalitis virus. Vaccine 2008; 26:2020-33. [PMID: 18339459 PMCID: PMC2465211 DOI: 10.1016/j.vaccine.2008.02.009] [Citation(s) in RCA: 43] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/02/2007] [Revised: 01/23/2008] [Accepted: 02/04/2008] [Indexed: 12/30/2022]
Abstract
West Nile virus (WNV) is a mosquito borne, neurotropic flavivirus that causes a severe central nervous system (CNS) infection in humans and animals. Although commercial vaccines are available for horses, none is currently approved for human use. In this study, we evaluated the efficacy and mechanism of immune protection of two candidate WNV vaccines in mice. A formalin-inactivated WNV vaccine induced higher levels of specific and neutralizing antibodies compared to a DNA plasmid vaccine that produces virus-like particles. Accordingly, partial and almost complete protection against a highly stringent lethal intracranial WNV challenge were observed in mice 60 days after single dose immunization with the DNA plasmid and inactivated virus vaccines, respectively. In mice immunized with a single dose of DNA plasmid or inactivated vaccine, antigen-specific CD8(+) T cells were induced and contributed to protective immunity as acquired or genetic deficiencies of CD8(+) T cells lowered the survival rates. In contrast, in boosted animals, WNV-specific antibody titers were higher, survival rates after challenge were greater, and an absence of CD8(+) T cells did not appreciably affect mortality. Overall, our experiments suggest that in mice, both inactivated WNV and DNA plasmid vaccines are protective after two doses, and the specific contribution of antibody and CD8(+) T cells to vaccine immunity against WNV is modulated by the prime-boost strategy.
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Affiliation(s)
- Bimmi Shrestha
- Department of Medicine, 660 S. Euclid Avenue, Box 8051, Washington University School of Medicine, St. Louis, MO 63110, United States
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15
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Abstract
West Nile virus (WNV) infection of mosquitoes, birds, and vertebrates continues to spread in the Western Hemisphere. In humans, WNV infects the central nervous system and causes severe disease, primarily in the immunocompromised and elderly. In this review we discuss the mechanisms by which antibody controls WNV infection. Recent virologic, immunologic, and structural experiments have enhanced our understanding on how antibodies neutralize WNV and protect against disease. These advances have significant implications for the development of novel antibody-based therapies and targeted vaccines.
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16
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Safety and efficacy in geese of a PER.C6-based inactivated West Nile virus vaccine. Vaccine 2007; 25:8338-45. [DOI: 10.1016/j.vaccine.2007.09.055] [Citation(s) in RCA: 25] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/02/2007] [Revised: 09/04/2007] [Accepted: 09/15/2007] [Indexed: 11/19/2022]
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Schepp-Berglind J, Luo M, Wang D, Wicker JA, Raja NU, Hoel BD, Holman DH, Barrett ADT, Dong JY. Complex adenovirus-mediated expression of West Nile virus C, PreM, E, and NS1 proteins induces both humoral and cellular immune responses. CLINICAL AND VACCINE IMMUNOLOGY : CVI 2007; 14:1117-26. [PMID: 17634508 PMCID: PMC2043313 DOI: 10.1128/cvi.00070-07] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 10/23/2022]
Abstract
West Nile Virus (WNV), a member of the family Flaviviridae, was first identified in Africa in 1937. In recent years, it has spread into Europe and North America. The clinical manifestations of WNV infection range from mild febrile symptoms to fatal encephalitis. Two genetic lineages (lineages I and II) are recognized; lineage II is associated with mild disease, while lineage I has been associated with severe disease, including encephalitis. WNV has now spread across North America, significantly affecting both public and veterinary health. In the efforts to develop an effective vaccine against all genetic variants of WNV, we have studied the feasibility of inducing both neutralizing and cellular immune responses by de novo synthesis of WNV antigens using a complex adenoviral vaccine (CAdVax) vector. By expressing multiple WNV proteins from a single vaccine vector, we were able to induce both humoral and cellular immune responses in vaccinated mice. Neutralization assays demonstrated that the antibodies were broadly neutralizing against both lineages of WNV, with a significant preference for the homologous lineage II virus. The results from this study show that multiple antigens synthesized de novo from a CAdVax vector are capable of inducing both humoral and cellular immune responses against WNV and that a multiantigen approach may provide broad protection against multiple genetic variants of WNV.
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Affiliation(s)
- Jennifer Schepp-Berglind
- Department of Microbiology and Immunology, Medical University of South Carolina, 173 Ashley Avenue, Charleston, SC 29403, USA
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18
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Okeson DM, Llizo SY, Miller CL, Glaser AL. ANTIBODY RESPONSE OF FIVE BIRD SPECIES AFTER VACCINATION WITH A KILLED WEST NILE VIRUS VACCINE. J Zoo Wildl Med 2007; 38:240-4. [PMID: 17679507 DOI: 10.1638/1042-7260(2007)038[0240:arofbs]2.0.co;2] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022] Open
Abstract
West Nile virus has been associated with numerous bird mortalities in the United States since 1999. Five avian species at three zoological parks were selected to assess the antibody response to vaccination for West Nile virus: black-footed penguins (Spheniscus demersus), little blue penguins (Eudyptula minor), American flamingos (Phoenicopterus ruber), Chilean flamingos (Phoenicopterus chilensis), and Attwater's prairie chickens (Tympanuchus cupido attwateri). All birds were vaccinated intramuscularly at least twice with a commercially available inactivated whole virus vaccine (Innovator). Significant differences in antibody titer over time were detected for black-footed penguins and both flamingo species.
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Affiliation(s)
- Danelle M Okeson
- Center for Conservation and Research, Henry Doorly Zoo, 3701 South Tenth Street, Omaha, Nebraska 68107, USA.
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19
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Dauphin G, Zientara S. West Nile virus: recent trends in diagnosis and vaccine development. Vaccine 2006; 25:5563-76. [PMID: 17292514 DOI: 10.1016/j.vaccine.2006.12.005] [Citation(s) in RCA: 111] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/17/2006] [Revised: 11/17/2006] [Accepted: 12/01/2006] [Indexed: 11/30/2022]
Abstract
West Nile virus (WNV) is a mosquito-borne flavivirus, native to Africa, Europe, and Western Asia. In many respects, WNV is an outstanding example of a zoonotic pathogen that has leaped geographical barriers and can cause severe disease in human and horse. Before the emergence of WNV in the USA, only few methods of diagnosis were available. Recently, many changes in the fields of WN diagnosis and prevention have happened. This paper will review all these new tools. After a description of the main concerns in WNV and West Nile (WN) disease in humans and animals, this review will present the main available tests for serology and virology detection, from gold standard tests to more recently developed methods. Finally, licensed vaccines and candidate vaccines developed in humans, horses and birds will also been described.
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Affiliation(s)
- G Dauphin
- AFSSA Alfort, UMR1161 (INRA-AFSSA-ENVA), 23 av Général de Gaulle, 94703 Maisons-Alfort Cedex, France
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Choi KS, Ko YJ, Nah JJ, Kim YJ, Kang SY, Yoon KJ, Joo YS. Monoclonal antibody-based competitive enzyme-linked immunosorbent assay for detecting and quantifying West Nile virus-neutralizing antibodies in horse sera. CLINICAL AND VACCINE IMMUNOLOGY : CVI 2006; 14:134-8. [PMID: 17135450 PMCID: PMC1797797 DOI: 10.1128/cvi.00322-06] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/20/2022]
Abstract
A rapid immunoassay for detecting and quantifying West Nile virus (WNV)-neutralizing antibodies in sera was developed as an alternative to the plaque reduction neutralization test (PRNT), the gold standard test for WNV. The assay is a competitive, enzyme-linked immunosorbent assay using neutralizing monoclonal antibody 5E8 (NT-ELISA). A cutoff percent inhibition (PI) value of 35% (mean PI plus 3 standard deviations), with a specificity of 99%, was established based on analysis of 246 serum samples from horses free of WNV. The NT-ELISA detected neutralizing antibodies in all sera collected 7 or 14 days postinoculation from mice (n = 11) infected with lineage I (strain NY385-99) or II (strain B956) WNV. When sera from WNV-vaccinated horses (n = 212) were tested by NT-ELISA and PRNT, the NT-ELISA gave a positive result for 96.1% (173/180) of the PRNT-positive sera and 3.1% (1/32) of the PRNT-negative sera. Discrepancies between the two tests were observed mainly with sera with low PRNT(90) titers (expressed as the reciprocal of the highest dilution yielding > or = 90% reduction in the number of plaques) for WNV or low PIs by NT-ELISA. The overall agreement (k value) between the two tests was 0.86. A good correlation (r(2) = 0.77) was also observed between the tests for endpoint titration of sera (n = 116). In conclusion, the newly developed NT-ELISA may be a good alternative serologic assay for detecting WNV that can be used for large-scale testing of WNV-neutralizing antibodies in multiple species.
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Affiliation(s)
- Kang-Seuk Choi
- National Veterinary Research and Quarantine Service, 480 Anyang-6 dong, Anyang, Gyeonggi 430-824, Republic of Korea.
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Siegal-Willott JL, Carpenter JW, Glaser AL. Lack of Detectable Antibody Response in Greater Flamingos (Phoenicopterus ruber ruber) After Vaccination Against West Nile Virus With a Killed Equine Vaccine. J Avian Med Surg 2006. [DOI: 10.1647/2005-005r.1] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022]
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Samina I, Khinich Y, Simanov M, Malkinson M. An inactivated West Nile virus vaccine for domestic geese-efficacy study and a summary of 4 years of field application. Vaccine 2005; 23:4955-8. [PMID: 16023273 DOI: 10.1016/j.vaccine.2005.03.052] [Citation(s) in RCA: 29] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/20/2004] [Revised: 10/17/2004] [Accepted: 03/07/2005] [Indexed: 12/27/2022]
Abstract
Following the isolation in 1997 of West Nile virus from the brains of geese with an acute neuroparalytic disease in Israel, which reappeared in the following years, an inactivated vaccine was prepared from suckling mouse brains. The brain homogenate was inactivated with formaldehyde and blended with mineral oil adjuvant. In 2000, the first flocks were vaccinated according to a schedule of two subcutaneous doses, commencing at the age of 2 weeks and given with a 2-weeks interval. In efficacy trials, the challenge virus was injected at 7 weeks by the intracranial route, and over 85% protection was recorded in vaccinated geese. In extensive field trials conducted in 2001--2003, the vaccine was demonstrated to be safe and efficacious, and over 3 million doses were manufactured in 2000--2003.
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Affiliation(s)
- Itzchak Samina
- Kimron Veterinary Institute, P.O. Box 12, Beit Dagan 50250, Israel.
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Abstract
West Nile virus (WNV) is a mosquito-borne flavivirus that is emerging as a global pathogen. In the last decade, virulent strains of the virus have been associated with significant outbreaks of human and animal disease in Europe, the Middle East and North America. Efforts to develop human and veterinary vaccines have taken both traditional and novel approaches. A formalin-inactivated whole virus vaccine has been approved for use in horses. DNA vaccines coding for the structural WNV proteins have also been assessed for veterinary use and have been found to be protective in mice, horses and birds. Live attenuated yellow fever WNV chimeric vaccines have also been successful in animals and are currently undergoing human trials. Additional studies have shown that immunisation with a relatively benign Australian variant of WNV, the Kunjin virus, also provides protective immunity against the virulent North American strain. Levels of efficacy and safety, as well as logistical, economic and environmental issues, must all be carefully considered before vaccine candidates are approved and selected for large-scale manufacture and distribution.
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Affiliation(s)
- Roy A Hall
- Department of Microbiology and Parasitology, The University of Queensland, Brisbane, Queensland 4072, Australia.
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Gancz AY, Barker IK, Lindsay R, Dibernardo A, McKeever K, Hunter B. West Nile virus outbreak in North American owls, Ontario, 2002. Emerg Infect Dis 2004; 10:2135-42. [PMID: 15663850 PMCID: PMC3323370 DOI: 10.3201/eid1012.040167] [Citation(s) in RCA: 44] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/19/2022] Open
Abstract
From July to September 2002, an outbreak of West Nile virus (WNV) caused a high number of deaths in captive owls at the Owl Foundation, Vineland, Ontario, Canada. Peak death rates occurred in mid-August, and the epidemiologic curve resembled that of corvids in the surrounding Niagara region. The outbreak occurred in the midst of a louse fly (Icosta americana, family Hippoboscidae) infestation. Of the flies tested, 16 (88.9 %) of 18 contained WNV RNA. Species with northern native breeding range and birds >1 year of age were at significantly higher risk for WNV-related deaths. Species with northern native breeding range and of medium-to-large body size were at significantly higher risk for exposure to WNV. Taxonomic relations (at the subfamily level) did not significantly affect exposure to WNV or WNV-related deaths. Northern native breeding range and medium-to-large body size were associated with earlier death within the outbreak period. Of the survivors, 69 (75.8 %) of 91 were seropositive for WNV.
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Affiliation(s)
- Ady Y Gancz
- University of Guelph, Guelph, Ontario, Canada.
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25
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Abstract
The Flaviviridae is a family of arthropod-borne, enveloped, RNA viruses that contain important human pathogens such as yellow fever (YF), Japanese encephalitis (JE), tick-borne encephalitis (TBE), West Nile (WN), and the dengue (DEN) viruses. Vaccination is the most effective means of disease prevention for these viral infections. A live-attenuated vaccine for YF, and inactivated vaccines for JE and TBE have significantly reduced the incidence of disease for these viruses, while licensed vaccines for DEN and WN are still lacking despite a significant disease burden associated with these infections. This review focuses on inactivated and recombinant subunit vaccines (non-replicating protein vaccines) in various stages of laboratory development and human testing. A purified, inactivated vaccine (PIV) candidate for DEN will soon be evaluated in a phase 1 clinical trial, and a second-generation JE PIV produced using similar technology has advanced to phase 2/3 trials. The inactivated TBE vaccine used successfully in Europe for almost 30 years continues to be improved by additional purification, new stabilizers, an adjuvant, and better immunization schedules. The recent development of an inactivated WN vaccine for domestic animals demonstrates the possibility of producing a similar vaccine for human use. Advances in flavivirus gene expression technology have led to the production of several recombinant subunit antigen vaccine candidates in a variety of expression systems. Some of these vaccines have shown sufficient promise in animal models to be considered as candidates for evaluation in clinical trials. Feasibility of non-replicating flavivirus vaccines has been clearly demonstrated and further development is now warranted.
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Affiliation(s)
- Kenneth H Eckels
- Division of Communicable Diseases and Immunology, Walter Reed Army Institute of Research, Silver Spring, Maryland 20910, USA
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Diamond MS, Shrestha B, Mehlhop E, Sitati E, Engle M. Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus. Viral Immunol 2004; 16:259-78. [PMID: 14583143 DOI: 10.1089/088282403322396082] [Citation(s) in RCA: 144] [Impact Index Per Article: 6.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/01/2023] Open
Abstract
WNV continues to spread throughout the Western Hemisphere as virus activity in insects and animals has been reported in the United States, Canada, Mexico, and the Caribbean islands. West Nile virus (WNV) infects the central nervous system and causes severe disease primarily in humans who are immunocompromised or elderly. In this review, we discuss the mechanisms by which the immune system limits dissemination of WNV infection. Recent experimental studies in animals suggest important roles for both the innate and the adaptive immune responses in controlling WNV infection. Interferons, antibody, complement components and CD8+ T cells coordinate protection against severe infection and disease. These findings are analyzed in the context of recent approaches to vaccine development and immunotherapy against WNV.
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Affiliation(s)
- Michael S Diamond
- Department of Medicine, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
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Hall RA, Broom AK, Smith DW, Mackenzie JS. The ecology and epidemiology of Kunjin virus. Curr Top Microbiol Immunol 2002; 267:253-69. [PMID: 12082993 DOI: 10.1007/978-3-642-59403-8_13] [Citation(s) in RCA: 51] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/25/2023]
Affiliation(s)
- R A Hall
- Department of Microbiology and Parasitology, School of Molecular and Microbial Sciences, The University of Queensland, St. Lucia, Queensland 4072, Australia
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