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      Bluetongue Serotype 3 in Israel 2013–2018: Clinical Manifestations of the Disease and Molecular Characterization of Israeli Strains

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          Abstract

          In this paper, the results of the diagnostic activities on Bluetongue virus serotype 3 (BTV-3) conducted at Kimron Veterinary Institute (Beit Dagan, Israel) between 2013 and 2018 are reported. Bluetongue virus is the causative agent of bluetongue (BT), a disease of ruminants, mostly transmitted by competent Culicoides species. In Israel, BTV-3 circulation was first detected in 2013 from a sheep showing classical BT clinical signs. It was also evidenced in 2016, and, since then, it has been regularly detected in Israeli livestock. Between 2013 and 2017, BTV-3 outbreaks were limited in sheep flocks located in the southern area only. In 2018, BTV-3 was instead found in the Israeli coastal area being one of the dominant BTV serotypes isolated from symptomatic sheep, cattle and goats. In Israeli sheep, BTV-3 was able to cause BT classical clinical manifestations and fatalities, while in cattle and goats infection ranged from asymptomatic forms to death cases, depending on either general welfare of the herds or on the occurrence of viral and bacterial co-infections. Three different BTV-3 strains were identified in Israel between 2013 and 2018: ISR-2019/13 isolated in 2013, ISR-2153/16 and ISR-2262/2/16 isolated in 2016. Sequencing and phylogenetic analysis of these strains showed more than 99% identity by segment (Seg) 2, 5, 6, 7, and 8 sequences. In contrast, a wide range of diversity among these strains was exhibited in other viral gene segments, implying the occurrence of genome reassortment between these local circulating strains and those originating from Africa. The genome sequences of the BTV-3 isolated in 2017 and 2018 were most closely related to those of the ISR-2153/16 strain suggesting their common ancestor. Comparison of BTV-3 Israeli strains with those recently detected in the Mediterranean region uncovered high percentage identity (98.19–98.28%) only between Seg-2 of all Israeli strains and the BTV-3 Zarzis/TUN2016 strain. A 98.93% identity was also observed between Seg-4 sequences of ISR-2019/13 and the BTV-3 Zarzis/TUN2016 strain. This study demonstrated that BTV-3 has been circulating in the Mediterranean region at least since 2013, but, unlike the other Mediterranean strains, Israeli BTV-3 were able to cause clinical signs also in cattle.

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          Most cited references38

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          The pathology and pathogenesis of bluetongue.

          Bluetongue (BT) is an insect-transmitted viral disease of wild and domestic ruminants and, occasionally, other species. Amongst domestic livestock, BT is most common in certain breeds of sheep whereas asymptomatic BT virus (BTV) infection of cattle is typical in enzootic regions. BT in cattle can be a feature of specific outbreaks, notably the current epizootic in Europe caused by BTV serotype 8. BTV replicates within mononuclear phagocytic and endothelial cells, lymphocytes and possibly other cell types in lymphoid tissues, the lungs, skin and other tissues. Infected ruminants may exhibit a prolonged but not persistent viraemia and BTV is associated with erythrocytes during the late stages of this prolonged viraemia. The pathogenesis of BT involves injury to small blood vessels in target tissues, but the relative contributions of direct virus-induced cytolysis and virus-induced vasoactive mediators in causing endothelial injury and dysfunction are presently unclear. The lesions of BT are characteristic and include: haemorrhage and ulcers in the oral cavity and upper gastrointestinal tract; necrosis of skeletal and cardiac muscle; coronitis; subintimal haemorrhage in the pulmonary artery; oedema of the lungs, ventral subcutis, and fascia of the muscles of the neck and abdominal wall; and pericardial, pleural and abdominal effusions. Transplacental transmission of BTV in ruminants, with subsequent fetal infection, is a property of specific virus strains, especially those propagated in embryonated eggs or cell culture. The outcome of BTV infection of fetal ruminants is age-dependent, with distinctive cavitating lesions of the central nervous system in animals that survive infection in early gestation. Immune competence to BTV arises by mid-gestation, and animals infected in late gestation can be born viraemic and without significant brain malformations.
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            Culicoides and the emergence of bluetongue virus in northern Europe.

            In June 2006, bluetongue virus, an arboviral pathogen of ruminants, appeared in northern Europe for the first time, successfully overwintered and subsequently caused substantial losses to the farming sector in 2007 and 2008. This emergence served as a test of how the probability of arboviral incursion into new regions is assessed and has highlighted the reliance of decision making on paradigms that are not always underpinned by basic biological data. In this review, we highlight those areas of the epidemiology of bluetongue that are poorly understood, reflect upon why certain vital areas of research have received little attention and, finally, examine strategies that could aid future risk assessment and intervention.
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              Development of a one-run real-time PCR detection system for pathogens associated with bovine respiratory disease complex

              Bovine respiratory disease complex (BRDC) is frequently found in cattle worldwide. The etiology of BRDC is complicated by infections with multiple pathogens, making identification of the causal pathogen difficult. Here, we developed a detection system by applying TaqMan real-time PCR (Dembo respiratory-PCR) to screen a broad range of microbes associated with BRDC in a single run. We selected 16 bovine respiratory pathogens (bovine viral diarrhea virus, bovine coronavirus, bovine parainfluenza virus 3, bovine respiratory syncytial virus, influenza D virus, bovine rhinitis A virus, bovine rhinitis B virus, bovine herpesvirus 1, bovine adenovirus 3, bovine adenovirus 7, Mannheimia haemolytica, Pasteurella multocida, Histophilus somni, Trueperella pyogenes, Mycoplasma bovis and Ureaplasma diversum) as detection targets and designed novel specific primer-probe sets for nine of them. The assay performance was assessed using standard curves from synthesized DNA. In addition, the sensitivity of the assay was evaluated by spiking solutions extracted from nasal swabs that were negative by Dembo respiratory-PCR for nucleic acids of pathogens or synthesized DNA. All primer-probe sets showed high sensitivity. In this study, a total of 40 nasal swab samples from cattle on six farms were tested by Dembo respiratory-PCR. Dembo respiratory-PCR can be applied as a screening system with wide detection targets.
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                Author and article information

                Contributors
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                06 March 2020
                2020
                : 7
                : 112
                Affiliations
                [1] 1Department of Virology, Kimron Veterinary Institute , Bet Dagan, Israel
                [2] 2OIE Reference Laboratory for Bluetongue, Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise (IZSAM), Campo Boario , Teramo, Italy
                [3] 3Hachaklait Veterinary Services , Caesarea, Israel
                [4] 4Indi-Vet Ltd. , Ashdod, Israel
                Author notes

                Edited by: Jesus Hernandez, Centro de Investigación en Alimentación y Desarrollo (CIAD), Mexico

                Reviewed by: Semmannan Kalaiyarasu, ICAR-National Institute of High Security Animal Diseases (ICAR-NIHSAD), India; Muhammad Zubair Shabbir, University of Veterinary and Animal Sciences, Pakistan

                *Correspondence: Natalia Golender golendern@ 123456moag.gov.il

                This article was submitted to Veterinary Infectious Diseases, a section of the journal Frontiers in Veterinary Science

                Article
                10.3389/fvets.2020.00112
                7068852
                d30a1157-a991-401b-aca2-7a67d5e41907
                Copyright © 2020 Golender, Bumbarov, Eldar, Lorusso, Kenigswald, Varsano, David, Schainin, Dagoni, Gur, Kaplan, Gorohov, Koren, Oron, Khinich, Sclamovich, Meir and Savini.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 September 2019
                : 13 February 2020
                Page count
                Figures: 2, Tables: 6, Equations: 0, References: 57, Pages: 14, Words: 9547
                Funding
                Funded by: Horizon 2020 10.13039/501100007601
                Categories
                Veterinary Science
                Original Research

                orbivirus,sheep,cattle,clinical signs,phylogeny,descriptive epidemiology

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