Influenza A in Bovine Species: A Narrative Literature Review

Abstract

It is quite intriguing that bovines were largely unaffected by influenza A, even though most of the domesticated and wild animals/birds at the human-animal interface succumbed to infection over the past few decades. Influenza A occurs on a very infrequent basis in bovine species and hence bovines were not considered to be susceptible hosts for influenza until the emergence of influenza D. This review describes a multifaceted chronological review of literature on influenza in cattle which comprises mainly of the natural infections/outbreaks, experimental studies, and pathological and seroepidemiological aspects of influenza A that have occurred in the past. The review also sheds light on the bovine models used in vitro and in vivo for influenza-related studies over recent years. Despite a few natural cases in the mid-twentieth century and seroprevalence of human, swine, and avian influenza viruses in bovines, the evolution and host adaptation of influenza A virus (IAV) in this species suffered a serious hindrance until the novel influenza D virus (IDV) emerged recently in cattle across the world. Supposedly, certain bovine host factors, particularly some serum components and secretory proteins, were reported to have anti-influenza properties, which could be an attributing factor for the resilient nature of bovines to IAV. Further studies are needed to identify the host-specific factors contributing to the differential pathogenetic mechanisms and disease progression of IAV in bovines compared to other susceptible mammalian hosts.

Keywords: Influenza A; MDBK cells; bovine; bovine cell cultures; bovine respiratory disease; bronchopneumonia; cattle outbreaks; epizootic cough; host restriction; ruminants; seroprevalence.

Figure 1

Schematic illustration of the literature search strategy. (A) A literature search was conducted using different keyword combinations in the PubMed database. Initial screening was carried out by shortlisting articles that matched the title for topic relevance and the availability of the articles in full text or abstract as shown in the flow chart. (B) Articles obtained after the keyword search were categorized based on their content as described in the pie chart. A comprehensive analyses of influenza A related studies in bovines represented by donut chart were conducted. Abbreviations used: Influenza A virus, IAV; Influenza B virus, IBV; Influenza C virus, ICV; Influenza D virus, IDV.

Figure 2

The host range for all four types (IAV, IBV, ICV, and IDV) of influenza viruses. The association of influenza disease in different mammalian species with reference to cattle (orange) is described separately. In each box, the bold black line represents active infection/disease; dotted black line represents the exposure without active infection/disease, as demonstrated by the serological evidence. A red dotted line in IAV indicates the possible source/routes of IAV infection (human, avian or swine) that can occur in bovines. Red blocked line indicates neither disease nor exposure. Vector graphic images used in the figure were taken from icon pool of the Microsoft Office and Freepik (www.freepik.com).

Figure 3

History timeline of the major influenza events in the past (A) Known human influenza pandemics along with the important outbreaks/discoveries. All the pandemics with year and country of origin are indicated in “black” flag, black font, while the other outbreaks/epidemics/discoveries are indicated in “orange” flag, red font. (B) influenza A incidences occurred in ruminants especially bovine species, were plotted based on the information from peer-reviewed articles. Only the natural infections/outbreaks and seroepidemiological studies reported in cattle in the past were included in the timeline. Experimental studies were excluded in this timeline. Illustrated major events included the major influenza outbreaks, cattle epizootics/respiratory disease with year and country of origin, and are represented by black triangle blocks, black font. Please note that both the timelines (A and B) have same dimensions starting with human pandemic as early as 1580 to 2013 H7N9 outbreaks and the timeframe of these cattle outbreaks/diseases (1889, 1893, 1914–1916, 1949, 1959–1960, 1971–1981, 1997–1999, 2005–2006) occurred almost concurrent to the human pandemic/outbreaks, which is indicative of the natural susceptibility of bovines to human influenza viruses. Most of the cattle influenza A isolates appeared to be related to human influenza A strains, with the HA glycoprotein similar to the prototypic human H2 and H3 subtypes.