A large-scale serological survey of Akabane virus infection in cattle, yak, sheep and goats in China

Highlights

• Cattle, sheep, goat and yak sera collected from across China were tested for neutralising antibody to Akabane virus (AKAV).

• AKAV neutralising antibody was detected in 23 of 24 provinces sampled (2006–2014).

• Overall seroprevalence rates were 21.3% in cattle (471/2215) and 12.0% in sheep/goats (17/142); there was no evidence of AKAV infection in yak (0/374).

• Neutralising antibodies to Aino virus and Peaton virus (but not five other Simbu group bunayviruses or closely related Leanyer virus) were also detected but only in a selection of AKAV-positive sera.

Abstract

Akabane virus (AKAV) is a member of the Simbu serogroup, classified in the genus Orthobunyavirus, family Bunyaviridae. AKAV infection can cause abortion, stillbirth, and congenital arthrogryposis and hydranencephaly in cattle and sheep. The distribution and prevalence of AKAV infection in China is still unknown. A total of 2731 sera collected from 2006 to 2015 in 24 provinces of China from cattle, sheep, goats and yak were examined by serum neutralisation test. The overall seroprevalence rates for AKAV antibodies were 21.3% in cattle (471/2215) and 12.0% (17/142) in sheep or goats, and 0% in yak (0/374). The results indicated widespread AKAV infection in China among cattle and sheep but yak appear to have a low risk of infection. Using a selection of 50 AKAV-positive and 25 AKAV-negative cattle sera, neutralisation tests were also conducted to detect antibodies to several other Simbu serogroup bunyaviruses and closely related Leanyer virus. Although inconclusive, the data suggest that both Aino virus and Peaton virus, which have been reported previously in Japan and Korea, may also be present in cattle in China.

Introduction

Akabane virus (AKAV) is a segmented, negative-sense, single-stranded RNA virus. It is classified taxonomically in the genus Orthobunyavirus, family Bunyaviridae (Plyusnin et al., 2012) and, like Schmallenberg virus (SBV) which emerged in 2011, it is a member of the Simbu serogroup of orthobunyaviruses (Hoffmann et al., 2012, Kinney and Calisher, 1981). AKAV has been isolated on several occasions from mosquitoes but biting midges (Culicoides spp.) appear to be the principal vectors (Jennings and Mellor, 1989). AKAV infects a wide range of wild ruminants and livestock including cattle, sheep, goats, buffalo, deer, horses and pigs (Kirkland, 2002, Huang et al., 2003). However, Akabane disease occurs primarily in cattle, and more rarely sheep and goats, manifesting as abortions, stillbirths and congenital abnormalities in newborns. Clinical signs include arthrogryposis and hydranencephaly (A–H syndrome), with the highest incidence and severity of disease when infection occurs during the mid-term of gestation. Post-natal infection of calves with some strains of the virus can also cause encephalomyelitis (Oem et al., 2012a, Oem et al., 2012b). There has been no report of AKAV infection in humans (Kirkland, 2002).

AKAV is known to be widely distributed across tropical and subtropical areas of East Asia as well as Australia, the Middle-East and Africa (Cybinski et al., 1978, Taylor and Mellor, 1994). The virus was first isolated from mosquitoes (Aedes vexans and Culex tritaeniorhynchus) collected in 1959 in Gumma Prefecture, Japan (Oya et al., 1961). Although the collection occurred during an outbreak of disease resulting in congenital malformation in cattle, an etiological link between the virus and this disease was not proposed until much later (Kurogi et al., 1975). A similar serious outbreak in Japan from 1972 to 1973 resulted in more than 31,000 cases of abortion, stillbirth and congenital A-H syndrome; the outbreak continued through 1974–1975 (Kurogi et al., 1975). AKAV was subsequently isolated from biting midges (Culicoides brevitarsis) in Australia in 1968 and an association between neutralising antibodies to AKAV and A-H syndrome in New South Wales was reported (Doherty et al., 1972, Hartley et al., 1975). AKAV isolations from cattle or biting midges have since been reported from Japan (Kurogi et al., 1987), Australia (St George et al., 1978), Chinese Taipei (Liao et al., 1996) and South Korea (Bak et al., 1980). Molecular detection of AKAV RNA has also been detected from biting midges and affected animals in Israel (Stram et al., 2004) and Turkey (Oğuzoğlu et al., 2015).

AKAV is also known to occur in China but the distribution, prevalence of infection and impacts on the cattle industry are poorly understood. The periodic and seasonal occurrence of AKAV infections in Japan, Taiwan and Korea suggests that China may play an important role epidemiologically in East Asia but virus distribution and epidemiology have been rarely reported. AKAV was first isolated in China in 1998 from mosquitos collected during a disease outbreak in Shanghai (Qiping and Longtao, 2000). This followed local reports in previous years of Akabane disease outbreaks in Shanghai, Guangdong, Henan, Shandong and Yunnan. A serological survey conducted in cattle and sheep in Xinjiang Province in north-west China in 2010 indicated a seroprevalence of 19% (Jun et al., 2012). A second virus isolation from mosquitoes in Yunnan Province has also been reported (Feng et al., 2015). However, no detailed data about the epidemiology of AKAV in China have been available for these past 20 years.

In this study, we have surveyed for AKAV neutralising antibodies in sera collected from cattle, yak, sheep and goats across 24 provinces of China during the period August 2006 to September 2015. We also determined the specificity of virus neutralisation among eight Simbu serogroup or closely related orthobunyaviruses previously reported in the Eastern Hemisphere and screened a selection of Chinese cattle sera for evidence of neutralising antibodies to each of the viruses.