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Foot-and-Mouth Disease Virus-Associated Abortion and Vertical Transmission following Acute Infection in Cattle under Natural Conditions.

ABSTRACT: Foot-and-mouth disease (FMD) is a highly contagious and economically important viral disease of cloven-hoofed animals, including domestic and wild host species. During recent FMD outbreaks in India, spontaneous abortions were reported amongst FMD-affected and asymptomatic cows. The current study was an opportunistic investigation of these naturally occurring bovine abortions to assess causality of abortion and vertical transmission of FMDV from infected cows to fetuses. For this purpose, fetal tissue samples of eight abortuses (heart, liver, kidney, spleen, palatine tonsil, umbilical cord, soft palate, tongue, lungs, and submandibular lymph node) were collected and screened by various detection methods, including viral genome detection, virus isolation, and immunomicroscopy. Amongst these cases, gross pathological changes were observed in 3 abortuses. Gross pathological findings included blood-tinged peritoneal and pleural effusions and myocarditis. Hearts of infected calves had mild to moderate degeneration and necrosis of the myocardium with moderate infiltration by mixed inflammatory cells. Localization of FMDV antigen was demonstrated in lungs and soft palate by immunomicroscopy. FMDV serotype O viral genome was recovered from 7 of 8 cases. Infectious FMDV serotype O was rescued by chemical transfection of the total RNA extracted from three soft palate samples and was sequenced to confirm 100% identity of the VP1 (capsid) coding region with isolates collected from infected cattle during the acute phase of infection. Based upon these findings, it may be concluded that FMDV-associated abortion occurred among the infected pregnant cows included within this study and FMDV was subsequently transmitted vertically to fetuses. This is the first documentation of FMDV-associated abortions in cattle.

SUBMITTER: Ranjan R

PROVIDER: S-EPMC5157973 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Foot-and-Mouth Disease Virus-Associated Abortion and Vertical Transmission following Acute Infection in Cattle under Natural Conditions.

Ranjan Rajeev R Biswal Jitendra K JK Subramaniam Saravanan S Singh Karam Pal KP Stenfeldt Carolina C Rodriguez Luis L LL Pattnaik Bramhadev B Arzt Jonathan J

PloS one 20161215 12

Foot-and-mouth disease (FMD) is a highly contagious and economically important viral disease of cloven-hoofed animals, including domestic and wild host species. During recent FMD outbreaks in India, spontaneous abortions were reported amongst FMD-affected and asymptomatic cows. The current study was an opportunistic investigation of these naturally occurring bovine abortions to assess causality of abortion and vertical transmission of FMDV from infected cows to fetuses. For this purpose, fetal t ...[more]

PMID: 27977708

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Project description:Foot-and-mouth disease (FMD), caused by FMD virus (FMDV; Aphthovirus, Picornaviridae), is a highly contagious and economically important disease of cloven-hoofed domestic livestock and wildlife species worldwide. Subsequent to the clinical phase of FMD, a large proportion of FMDV-infected ruminants become persistently infected carriers, defined by detection of FMDV in oropharyngeal fluid (OPF) samples 28 days or more post-infection. The goal of this prospective study was to characterize the FMD carrier state in cattle subsequent to natural infection under typical husbandry practices in Vietnam. Ten persistently infected cattle on eight farms in the Long An province in southern Vietnam were monitored by monthly screening of serum and oropharyngeal fluid samples for 12 months. To assess transmission from FMDV carriers, 16 naïve cattle were intentionally brought into direct contact with the persistently infected animals for 6 months, and were monitored by clinical and laboratory methods. The restricted mean duration of the FMD carrier state was 27.7 months, and the rate of decrease of the proportion of carrier animals was 0.03 per month. There was no evidence of transmission to naïve animals throughout the study period. Additionally, there was no detection of FMDV infection or seroconversion in three calves born to carrier animals during the study. The force of infection for carrier-to-contact transmission was 0 per month, with upper 95% confidence limit of 0.064 per month. Phylogenetic analysis of viral protein 1 (VP1) coding sequences obtained from carriers indicated that all viruses recovered in this study belonged to the O/ME-SA/PanAsia lineage, and grouped phylogenetically with temporally and geographically related viruses. Analysis of within-host evolution of FMDV, based upon full-length open reading frame sequences recovered from consecutive samples from one animal, indicated that most of the non-synonymous changes occurred in Lpro, VP2, and VP3 protein coding regions. This study suggests that the duration of FMDV persistent infection in cattle may be longer than previously recognized, but the risk of transmission is low. Additional novel insights are provided into within-host viral evolution under natural conditions in an endemic setting.

Project description:Foot-and-mouth disease (FMD) is one of the most economically important livestock diseases worldwide. Following the clinical phase of FMD, a large proportion of ruminants remain persistently infected for extended periods. Although extinction of this carrier state occurs continuously at the animal and population levels, studies vary widely in their estimates of the duration of persistent infection. There is a need for robust statistical models to capture the dynamics of persistent infection for the sake of guiding FMD control and trade policies. The goal of the current study was to develop and assess statistical models to describe the extinction of FMD virus (FMDV) persistent infection using data from primary longitudinal studies of naturally infected cattle and Asian buffalo in Vietnam and India. Specifically, accelerated failure time (AFT) models and generalized linear mixed models (GLMM) were developed to predict the probability of persistent infection in seropositive animals and identified carriers at the individual animal level at sequential time points after outbreaks. The primary studies were analyzed by country and combined using an individual-participant data meta-analysis approach. The models estimated similar trends in the duration of persistent infection for the study/species groups included in the analyses, however the significance of the trends differed between the models. The overall probabilities of persistent infection were similar as predicted by the AFT and GLMM models: 6 months: 99% (AFT) /80% (GLMM), 12 months: 51% (AFT) /32% (GLMM), 18 months: 6% (AFT) /5% (GLMM), 24 months: 0.8% (AFT) /0.6% (GLMM). These models utilizing diverse and robust data sets predict higher probabilities of persistence than previously published, suggesting greater endurance of carriers subsequent to an outbreak. This study demonstrates the utility of statistical models to investigate the dynamics of persistent infection and the importance of large datasets, which can be achieved by combining data from several smaller studies in meta-analyses. Results of this study enhance current knowledge of the FMDV carrier state and may inform policy decisions regarding FMDV persistent infection.

Project description:Control and eradication of foot-and-mouth disease (FMD) are impeded by the existence of a persistent, subclinical phase of infection in ruminants; animals with this status are referred to as carriers. However, the epidemiological significance of these FMD virus (FMDV) carriers is uncertain. In the current investigation, the contagion associated with FMDV carrier cattle was investigated by exposure of susceptible cattle and pigs to oropharyngeal fluid (OPF) samples or tissues harvested from persistently infected cattle. Naive cattle were inoculated through intranasopharyngeal deposition of unprocessed OPF samples that had been collected from FMDV carriers at 30 days postinfection. These inoculated cattle developed clinical FMD, and the severity of disease they developed was similar to that of animals that had been infected with a high-titer inoculum. In contrast, pigs exposed via intraoropharyngeal inoculation of the same OPF samples or via ingestion of nasopharyngeal tissues harvested from the same cohort of persistently infected cattle did not develop FMD. These findings indicate that there is demonstrable contagion associated with FMDV carrier cattle despite the lack of evidence for transmission by direct contact. The findings presented herein provide novel information that should be considered for FMD risk mitigation strategies.IMPORTANCE Foot-and-mouth disease (FMD) is a viral disease of livestock with substantial impact on agricultural production and subsistence farming on a global scale. Control of FMD is impeded by the existence of a prolonged asymptomatic carrier phase during which infected cattle shed low quantities of infectious virus in oropharyngeal fluid (OPF) for months to years after infection. The epidemiological significance of FMD virus (FMDV) carriers is unresolved. However, the existence of the FMDV carrier state has substantial impact on international trade in animal products. The current investigation demonstrated that transfer of OPF from persistently infected FMDV carrier cattle to naive cattle led to fulminant clinical FMD. It was thus demonstrated that, although the risk for disease transmission under natural conditions is considered to be low, there is detectable contagion associated with FMDV carrier cattle. This finding is important for optimization of FMD risk mitigation strategies.

Project description:Foot-and-mouth disease (FMD) field studies have suggested the occurrence of simultaneous infection of individual hosts by multiple virus strains; however, the pathogenesis of foot-and-mouth disease virus (FMDV) coinfections is largely unknown. In the current study, cattle were experimentally exposed to two FMDV strains of different serotypes (O and A). One cohort was simultaneously infected with both viruses, while additional cohorts were initially infected with FMDV A and subsequently superinfected with FMDV O after 21 or 35 days. Coinfections were confirmed during acute infection, with both viruses concurrently detected in blood, lesions, and secretions. Staggered exposures resulted in overlapping infections as convalescent animals with persistent subclinical FMDV infection were superinfected with a heterologous virus. Staggering virus exposure by 21 days conferred clinical protection in six of eight cattle, which were subclinically infected following the heterologous virus exposure. This effect was transient, as all animals superinfected at 35 days post-initial infection developed fulminant FMD. The majority of cattle maintained persistent infection with one of the two viruses while clearing the other. Analysis of viral genomes confirmed interserotypic recombination events within 10 days in the upper respiratory tract of five superinfected animals from which the dominant genomes contained the capsid coding regions of the O virus and nonstructural coding regions of the A virus. In contrast, there were no dominant recombinant genomes detected in samples from simultaneously coinfected cattle. These findings inculpate persistently infected carriers as potential FMDV mixing vessels in which novel strains may rapidly emerge through superinfection and recombination. IMPORTANCE Foot-and-mouth disease (FMD) is a viral infection of livestock of critical socioeconomic importance. Field studies from areas of endemic FMD suggest that animals can be simultaneously infected by more than one distinct variant of FMD virus (FMDV), potentially resulting in emergence of novel viral strains through recombination. However, there has been limited investigation of the mechanisms of in vivo FMDV coinfections under controlled experimental conditions. Our findings confirmed that cattle could be simultaneously infected by two distinct serotypes of FMDV, with different outcomes associated with the timing of exposure to the two different viruses. Additionally, dominant interserotypic recombinant FMDVs were discovered in multiple samples from the upper respiratory tracts of five superinfected animals, emphasizing the potential importance of persistently infected FMDV carriers as sources of novel FMDV strains.

Project description:Nigeria is a large densely populated country in West Africa. Most of its livestock is raised in a pastoralist production system with typical long distance migration in search of water and feed. As the demand for animal products largely exceeds the domestic production, large numbers of livestock are imported from neighboring countries without sanitary restrictions. In Nigeria, foot-and-mouth disease virus (FMDV) serotypes O, A, and Southern African Territories (SAT)2 are endemic for a long time. Clinical outbreaks of FMD due to serotype SAT1 are described again since 2015, after an absence of more than 30 years. Historically, outbreaks of FMD due to serotypes O, A, SAT1, and SAT2 were each time associated with trade of cattle entering Nigeria from neighboring countries. In the present study, tissue samples from 27 outbreaks of FMD were collected in Nigerian cattle from 2012 until 2017 in six different States and in the Federal Capital Territory. FMDV was isolated and serotyped and further characterized by VP1 sequencing and phylogenetic analysis to gain more knowledge on FMDV circulation in Nigeria. Half of the outbreaks were characterized as FMDV topotype O/EA-3, while outbreaks with other serotypes and topotypes were-in descending order-less prevalent: A/Africa/G-IV, SAT1/X, SAT2/VII, and O/WA. The high dynamics and omnipresence of FMD in Nigeria were illustrated in Plateau State where FMDV serotypes O, SAT1, and SAT2 were isolated during the course of the study, while at some point in the study, outbreaks due to FMDV serotype A were observed in three remote States. The genetic and phylogenetic analysis suggests a mixed origin of FMD outbreaks. Some outbreaks seem to be caused by sustained local transmission of FMDV strains present in Nigeria since a number of years, while other outbreaks seem to be related to recent incursions with new FMDV strains. The role of African buffaloes in the etiology of FMD in Nigeria is unclear, and sampling of wildlife is needed. The results of the present study suggest that systematic sample collection is essential to understand the complex concomitance of FMDV strains in Nigeria and essential to support the implementation of a vaccination-based control plan.

Dataset Information

Foot-and-Mouth Disease Virus-Associated Abortion and Vertical Transmission following Acute Infection in Cattle under Natural Conditions.

Publications

Foot-and-Mouth Disease Virus-Associated Abortion and Vertical Transmission following Acute Infection in Cattle under Natural Conditions.

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