Influenza D virus infection in Mississippi beef cattle

Ferguson, Lucas; Eckard, Laura; Epperson, William B.; Liang, Liping; Smith, David R.; Huston, Carla L.; Genova, Suzanne G.; Webby, Richard J.; Wan, Xiu‐Feng

doi:10.1016/j.virol.2015.08.030

Cited by 119 publications

(200 citation statements)

References 12 publications

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“…Our virologic surveillance found that IDV was present in 23.6% of 55 calves affected with BRD but in only 2.4% of 82 healthy calves upon arrival at the same facility (4). Other studies have shown that the IDV positivity rates in cattle with BRD in the United States and France were 4.5% and 4.8%, respectively (3,6).…”

mentioning

confidence: 43%

“…Viral RNA was extracted using a GeneJet viral DNA/RNA purification kit according to the manufacturer's protocol (Thermo Scientific, Pittsburgh, PA). Gene-specific amplification primers were designed according to the D/swine/1334/Oklahoma/2011 sequence and a reverse transcription (RT) primer based upon the conserved noncoding regions, as described previously (4).…”

Section: Methodsmentioning

confidence: 99%

“…The virus was recently detected in sheep and goats (8). Serological studies have shown that IDV has been present in beef cattle at least since 2004 (4). Cattle have been proposed as the reservoirs for IDV, and young, weaned, comingled, and immunologically naive calves seem to be most susceptible to infection due to dwindling maternal antibody levels after 6 months of age (4).…”

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confidence: 99%

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Pathogenesis of Influenza D Virus in Cattle

Ferguson

Olivier

Genova

et al. 2016

J Virol

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141

187

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Cattle have been proposed as the natural reservoir of a novel member of the virus family Orthomyxoviridae, which has been tentatively classified as influenza D virus (IDV). Although isolated from sick animals, it is unclear whether IDV causes any clinical disease in cattle. To address this aspect of Koch's postulates, three dairy calves (treatment animals) held in individual pens were inoculated intranasally with IDV strain D/bovine/Mississippi/C00046N/2014. At 1 day postinoculation, a seronegative calf (contact animal) was added to each of the treatment animal pens. The cattle in both treatment and contact groups seroconverted, and virus was detected in their respiratory tracts. Histologically, there was a significant increase in neutrophil tracking in tracheal epithelia of the treatment calves compared to control animals. While infected and contact animals demonstrated various symptoms of respiratory tract infection, they were mild, and the calves in the treatment group did not differ from the controls in terms of heart rate, respiratory rate, or rectal temperature. To mimic zoonotic transmission, two ferrets were exposed to a plastic toy fomite soaked with infected nasal discharge from the treatment calves. These ferrets did not shed the virus or seroconvert. In summary, this study demonstrates that IDV causes a mild respiratory disease upon experimental infection of cattle and can be transmitted effectively among cattle by in-pen contact, but not from cattle to ferrets through fomite exposure. These findings support the hypothesis that cattle are a natural reservoir for the virus. IMPORTANCE A novel influenza virus, tentatively classified as influenza D virus (IDV), was identified in swine, cattle, sheep, and goats. Among these hosts, cattle have been proposed as the natural reservoir. In this study, we show that cattle experimentally infected with IDV can shed virus and transmit it to other cattle through direct contact, but not to ferrets through fomite routes. IDV caused minor clinical signs in the infected cattle, fulfilling another of Koch's postulates for this novel agent, although other objective clinical endpoints were not different from those of control animals. Although the disease observed was mild, IDV induced neutrophil tracking and epithelial attenuation in cattle trachea, which could facilitate coinfection with other pathogens, and in doing so, predispose animals to bovine respiratory disease.

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confidence: 43%

Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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Pathogenesis of Influenza D Virus in Cattle

Ferguson

Olivier

Genova

et al. 2016

J Virol

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141

187

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“…Siedem segmentów genomu nowego wirusa koduje 9 białek wirusowych: glikoproteinę (białko fuzyjne hemaglutynino-esterazę, HE), polimerazy (PB 1, 2 i 3), NP, białka matriks (M1 i CM2) oraz białka niestrukturalne (NS1 i NEP) (5).…”

Section: Struktura Genomuunclassified

Characterization of a new influenza virus type D

Markowska-Daniel¹,

Mickiewicz²,

Witkowski³

et al. 2016

Medycyna Weterynaryjna

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Influenza is caused by viruses belonging to the Orthomyxoviridae family. Currently three types of influenza virus are known: A (Influenza A virus, IAV), B (IBV) and C (ICV). Despite the fact that all these viruses are derived from a common ancestor they differ from each other by the number of segments, the size and sequence of RNA segments, antigenicity, pathogenicity and the spectrum of natural reservoirs. In 2011, a new influenza virus was isolated in the USA from pigs manifesting influenza-like symptoms. The virus was the most closely related to ICV. It was able to replicate in vitro in different cell cultures and displayed much broader cell tropism than human ICV. Moreover, in contrast to ICV, it was able to replicate at 370C. Electron microscopic studies demonstrated features characteristic of Orthomyxoviruses. Despite morphological and organizational similarities, the biological properties of the new virus, including biochemical activity, differ from that of other influenza viruses. Enzymatic assays revealed that the new virus had negligible neuraminidase but detectable O-acetyloesterase activity. Further studies evidenced that the new virus varied from ICV in receptor binding, despite its sharing a conserved array of functional domains in the viral RNA genome replication and viral entry machinery. Analysis conducted with the use of the model of crystal structure of the hemagglutinin-esterase fusion protein (HE) of the new virus and its receptor demonstrated that this protein was multifunctional. It catalyzes cellular receptor binding, receptor cleavage, as well as membrane fusion. Moreover, divergent receptor-binding sites than HE of ICV have been discovered in the new virus. These amino acid differences may alter the binding specificity and affinity of the HE protein to the receptor that in turn result in the observed differences in cellular tropism between the two viruses. It also possesses an open channel between the 230-helix and 270-loop in the receptor-binding site, which is a unique feature of this virus. This might explain why the new virus has a broad cell tropism. It is possible that the sequence variation in the fusion domain may influence the replication of this virus at a higher temperature when compared to ICV. Next-generation sequencing demonstrated that the genome of the new virus, similarly to ICV, had seven single-stranded negative-sense RNA segments coding 9 viral proteins. Deep RNA sequencing found a M1 protein expression strategy different from that of ICV. Studies aimed at evaluating of the evolutionary relationship of both viruses revealed that the new virus and ICV shared an approximately 69-72% mean pairwise identity in the PB1 gene, which is reported to be the most conserved influenza virus protein. Additionally, differences were detected at 5’ and 3’ends of noncoding regions, which are also highly conserved. They both may be responsible for the lack of in vitro reassortment between ICV of human origin and the new virus. In the study characterizing antigenic properties of the new virus, no cross-reactivity was observed using HI and AGID tests. This indicates the major differences in conserved proteins M1 and NP between both viruses. Summing up, despite the fact that new virus is the most closely related to human ICV, the number of important antigenic and genetic distinctions among them is the basis for suggesting that the International Committee of Virus Taxonomy classify it as a separate genus - D. There is no doubt that the discovery of a new influenza virus genus will have a great impact on influenza research and ecology.

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“…Między innymi: nowy wirus posiada zdolność do replikacji in vitro w większej liczbie hodowli komórkowych niż ICV; różnił się powinowactwem do receptorów komórkowych, strukturą i miejscem wiązania białka fuzyjnego hemaglutynino-esterazy (HE) z receptorem; ekspresją białka matriks 1; sekwencją w regionach niekodujących; aktywnością neuraminidazy i O-acetyloesterazy; był zdolny do replikacji w temperaturze 37°C; nie dawał reakcji krzyżowych w testach serologicznych, a także nie ulegał reasortacji in vitro z ludzkimi szczepami ICV (2,5,6,22). Dowodzi to, że nowy wirus stanowi odrębny typ i z tego powodu jego szczep prototypowy przemianowano na D/swine/ Oklahoma/1334/2011 (D/OK).…”

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Prevalence of infections with a new type of influenza virus – influenza D virus in humans and animals

Markowska-Daniel¹,

Mickiewicz²,

Witkowski³

et al. 2016

Medycyna Weterynaryjna

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In April 2011, in the USA, a new influenza virus type D (IDV) was isolated for the first time from pigs and then from cows. In the paper the data about the prevalence of this virus in humans and animals are described. It was evidenced that HE protein of IDV could bind to cellular receptors in the epithelium of the human trachea. Moreover, the new virus was shown to infect and spread in ferrets. These findings make it possible to conclude that IDV seems to be able to infect humans and have zoonotic potential. Up to now the percent of human seroconverted to IDV has been low, about 1.3%. The susceptibility of pigs to IDV has been shown in natural and experimental conditions. Virus specific antibodies were detected in 9.5% of pigs. Additionally the isolates from pigs were obtained in the USA and Italy. This suggests that pigs are not the natural reservoir of this virus and the infections are uncommon in pig populations. Several studies demonstrated that the new virus is widely spread in cattle. It was isolated in the USA, Canada, China, France and Italy, which proved that the intercontinental transmission of IDV had occurred. The highest percentage of infected cows, mainly animals manifesting BRDC symptoms, was found in Minnesota, Oklahoma and Mississippi, and it varied from 4.8 to 29.1%. Additionally the virus was detected in 2.4% of healthy animals. Seroconversion was demonstrated in 32.7 to 87.5% of the bovine herds tested in Mississippi and Minnesota, respectively. Retrospective analysis revealed that antibodies specific to IDV had been detected in bovine samples since 2004. This suggests that the new virus has circulated in cattle at least since 2004. The analysis of the relationship between the seroconversion and the age of animals showed that over 50% of cows aged 1–14 years were seropositive. Also more than 90% of newborn calves had maternal antibodies to IDV. The spread of IDV was also linked to the type of farm, with the lowest percentage of animals seroconverting in closed herds and the highest in order-buying facilities. Therefore cattle seem to be the natural host of IDV. In the USA and Canada the infections caused by IDV were also found in sheep and goats. Herd-level and individual-level seroprevalence in sheep was 15.3 and 6.1%, respectively, and these figures were even higher in goats: 20% and 25.9%, respectively. This shows that small ruminants are susceptible to IDV infection. Moreover, retrospective analysis confirmed that one serum from a goat taken in Massachusetts in 2002 was positive to IDV. This suggests that the new virus may have circulated among goats as early as in 2002. Serological studies of chicken and turkey sera from the herds in Minnesota, located near the positive bovine herds, yielded negative results. This might suggest that birds are resistant to IDV infection; however, the number of birds tested is insufficient to substantiate such a statement. The studies aimed at evaluation of zoonotic potential of the new virus proved that it replicated efficiently in the upper respiratory tract of ferrets. This suggests that the new virus may have an influence on public health. In experimental conditions the susceptibility of guinea pigs to IDV infection was also evidenced. In conclusion, all the studies demonstrated that cattle were the natural reservoir of the new virus, despite the fact that humans as well as various animal species could also be infected. Furthermore, cattle are likely to be a potential source of infection for both animals and humans.

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Influenza D virus infection in Mississippi beef cattle

Cited by 119 publications

References 12 publications

Pathogenesis of Influenza D Virus in Cattle

Pathogenesis of Influenza D Virus in Cattle

Characterization of a new influenza virus type D

Prevalence of infections with a new type of influenza virus – influenza D virus in humans and animals

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