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      Time Course-Dependent Study on Equine Herpes Virus 9-Induced Abortion in Syrian Hamsters

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          Abstract

          Simple Summary

          Equine herpesvirus 9 (EHV-9) is a virus belonging to the family of equine herpesviruses. EHV-9 has been isolated from natural infections of different wild and zoo animals. In addition, it has been associated with encephalitis and abortion in several animal species. However, the host range and pathogenesis of this virus are still unknown. Herein, we investigated the underlying pathogenesis of EHV-9-induced abortion in relation to the gestation period in either early or late trimester infection. We noticed that the late trimester infection of EHV-9 was associated with more severe death and both placental and fetal tissue localization of the virus. Also, early stage infection was accompanied by band necrotic changes within the placenta, which usually led to abortion.

          Abstract

          This study aimed to follow the time-course pathogenesis of EHV-9 abortion in early and late trimesters. Twenty-seven pregnant hamster dams were divided into three groups: (G1) control, (G2) EHV-9-inoculated on the 5th day (early trimester), and (G3) EHV-9-inoculated on the 10th day of gestation (late trimester). Dams were sacrificed at different time points during gestation and examined for viremia and viral DNA in different fetal and maternal tissues and pathological changes in fetal tissue, placenta, and cytokines. Animals in G3 showed a marked increase in the number of dead fetuses than those in G2. Histopathological findings of G2 showed early band coagulative necrosis of maternal spaces and stromal decidual cells. Necrotic changes were observed within the decidua basalis, spongiotrophoblast layer, and labyrinth. First, the virus was localized within mononuclear leukocytes in the decidua capsularis and basalis, and within the necrotic chorionic villi and cervical epithelium. G3 demonstrated degenerative changes within the chorionic villi and trophospongium. The virus antigen was observed within the chorionic villi, trophoblasts, mononuclear cells, and fetal tissues. In conclusion, EHV-9 induced abortion mostly occurs through necrosis of the chorionic villi and cannot cross through the capsular placenta in the early trimester but can through the developed decidual placentation.

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          Most cited references45

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          Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis.

          Human cytomegalovirus (CMV) is the leading cause of prenatal viral infection. Affected infants may suffer intrauterine growth retardation and serious neurologic impairment. Analysis of spontaneously aborted conceptuses shows that CMV infects the placenta before the embryo or fetus. In the human hemochorial placenta, maternal blood directly contacts syncytiotrophoblasts that cover chorionic villi and cytotrophoblasts that invade uterine vessels, suggesting possible routes for CMV transmission. To test this hypothesis, we exposed first-trimester chorionic villi and isolated cytotrophoblasts to CMV in vitro. In chorionic villi, syncytiotrophoblasts did not become infected, although clusters of underlying cytotrophoblasts expressed viral proteins. In chorionic villi that were infected with CMV in utero, syncytiotrophoblasts were often spared, whereas cytotrophoblasts and other cells of the villous core expressed viral proteins. Isolated cytotrophoblasts were also permissive for CMV replication in vitro; significantly, infection subsequently impaired the cytotrophoblasts' ability to differentiate and invade. These results suggest two possible routes of CMV transmission to the fetus: (i) across syncytiotrophoblasts with subsequent infection of the underlying cytotrophoblasts and (ii) via invasive cytotrophoblasts within the uterine wall. Furthermore, the observation that CMV infection impairs critical aspects of cytotrophoblast function offers testable hypotheses for explaining the deleterious effects of this virus on pregnancy outcome.
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            Interferon-γ promotes abortion due to Brucella infection in pregnant mice

            Background The mechanisms of abortion induced by bacterial infection are largely unknown. In the present study, we investigated abortion induced by Brucella abortus, a causative agent of brucellosis and facultative intracellular pathogen, in a mouse model. Results High rates of abortion were observed for bacterial infection on day 4.5 of gestation, but not for other days. Regardless of whether fetuses were aborted or stayed alive, the transmission of bacteria into the fetus and bacterial replication in the placenta were observed. There was a higher degree of bacterial colonization in the placenta than in other organs and many bacteria were detected in trophoblast giant cells in the placenta. Intracellular growth-defective virB4 mutant and attenuated vaccine strain S19 did not induce abortion. In the case of abortion, around day 7.5 of gestation (period of placental development), transient induction of IFN-γ production was observed for infection by the wild type strain, but not by the virB4 mutant and S19. Neutralization of IFN-γ, whose production was induced by infection with B. abortus, served to prevent abortion. Conclusion These results indicate that abortion induced by B. abortus infection is a result of transient IFN-γ production during the period of placental development.
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              A survey of equine abortion, stillbirth and neonatal death in the UK from 1988 to 1997.

              A detailed review of laboratory records for equine abortion is fundamental in establishing current disease trends and suggesting problems important for further research. To review the causes of abortion and neonatal death in equine diagnostic submissions to the Animal Health Trust over a 10 year period. The diagnoses in 1252 equine fetuses and neonatal foals were reviewed and analysed into categories. Problems associated with the umbilical cord, comprising umbilical cord torsion and the long cord/cervical pole ischaemia disorder, were the most common diagnoses (38.8%: 35.7% umbilical cord torsion and 3.1% long cord/cervical pole ischaemia disorder). Other noninfective causes of abortion or neonatal death included twinning (6.0%), intrapartum stillbirth (13.7%) and placentitis, associated with infection (9.8%). E. coli and Streptococcus zooepidemicus were the most common bacteria isolated. Neonatal infections not associated with placentitis accounted for 3.2% of incidents; and infections with EHV-1 or EHV-4 for 6.5%. Definitive diagnosis of equine abortion is possible in the majority of cases where the whole fetus and placenta are submitted for examination. Given the high incidence of umbilical cord torsion and related problems as causes of abortion in UK broodmares, more research on factors determining umbilical cord length and risk of torsion is essential.
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                Author and article information

                Journal
                Animals (Basel)
                Animals (Basel)
                animals
                Animals : an Open Access Journal from MDPI
                MDPI
                2076-2615
                07 August 2020
                August 2020
                : 10
                : 8
                Affiliations
                [1 ]Department of Pathogenetic Veterinary Sciences, United Graduate School of Veterinary Sciences, Gifu University, Gifu 501-1193, Japan; dr_osamaabas2020@ 123456yahoo.com (O.A.); hfukushi@ 123456gifu-u.ac.jp (H.F.)
                [2 ]Department of Animal Medicine, Faculty of Veterinary Medicine, Alexandria University, 21526 Alexandria, Egypt
                [3 ]Department of Pathology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516 Kafrelsheikh, Egypt; waliedsobhy@ 123456yahoo.com
                [4 ]Department of Virology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516 Kafrelsheikh, Egypt; samykasem2@ 123456gmail.com
                [5 ]Department of Veterinary Diagnostic Laboratories, Ministry of Environment, Water and Agriculture, Riyadh 11195, Saudi Arabia; a.alwazzan83@ 123456gmail.com
                [6 ]Department of Animal Medicine, Faculty of Veterinary Medicine, Damanhur University, 22511 Damanhur, Egypt; dr_asmaaghalep@ 123456yahoo.com
                [7 ]Department of Pharmacology and Toxicology, Faculty of Pharmacy, Al-Azhar University, 11651 Cairo, Egypt; iisaleh44@ 123456gmail.com
                [8 ]Laboratory of Wildlife and Forensic Pathology, Biomedical Science Examination and Research Center, Department of Veterinary Medicine, Faculty of Veterinary Medicine, Okayama University of Science, Imabari, Ehime 794-8555, Japan
                [9 ]Department of Pathology and Clinical Pathology, Faculty of Veterinary Medicine, South Valley University, 83523 Qena, Egypt
                Author notes
                [* ]Correspondence: tokumayanai@ 123456gmail.com (T.Y.); mohieharidy@ 123456svu.edu.eg (M.H.); Tel./Fax: +81-58-293-2959 (T.Y.)
                Article
                animals-10-01369
                10.3390/ani10081369
                7459792
                32784541
                e5efae1e-8e01-4cc9-ba6e-a6e110f7e7cd
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                Categories
                Article

                ehv9,hamster,early and late trimester,cytokines,abortion
                ehv9, hamster, early and late trimester, cytokines, abortion

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