Nairobi sheep disease
Nairobi sheep disease (NSD) is a highly pathogenic disease of sheep and goats, causing acute haemorrhagic gastroenteritis in naïve animals. NSD has a limited effect on animals bred in endemic areas but large losses can occur when naïve animals are exposed to the virus. Originally limited to East Africa, NSD now occurs in most of Africa as well as Sri Lanka and India. More recently, a novel strain of NSD virus was sequenced from ticks in China.
NSD is listed as a notifiable disease by the World Organisation for Animal Health (OIE) and is on the Australian national list of notifiable animal diseases. Australia is free of NSD virus and has never had a reported case.
Aetiology
NSD virus is a member of the genus Nairovirus, family Bunyaviridae. Nairoviruses are tick-borne viruses that are classified into seven serogroups, the most important being the Crimean Congo Haemorrhagic Fever group and the NSD group1. NSD is highly pathogenic in naïve animals, with mortality up to 90%. However, it has not been seen as a threat in developed countries because it was believed to be restricted to Africa.
Distribution
NSD was first identified in sheep in Nairobi, Kenya in 1910 and is now present across east and central Africa as well as Uganda, Ethiopia, Somalia, Botswana and Mozambique. A similar disease caused by the closely related Ganjam virus has occurred in sheep and goats in India since the 1960s. Due to its occurrence on a different continent and association with different ticks, Ganjam virus was initially considered a separate virus from the one causing NSD. However, the serological cross-reactivity and relatively high sequence identity between NSD and Ganjam viruses have led to the proposal that Ganjam virus is an Asian variant of NSD virus rather than a distinct species2.
NSD virus was isolated from Haemaphysalis intermedia ticks in Sri Lanka in 19953 and viral RNA was found in Haemaphysalis longicornis ticks in China in 20134. This Chinese isolate is genetically divergent from both NSD virus in Africa and Ganjam virus in Asia. The increased use of modern molecular techniques has shown that the virus has a much wider distribution than previously suspected.
Transmission
NSD virus is transmitted by ticks. It is not transmitted between animals by direct contact. The primary tick vector in Africa is Rhipicephalus appendiculatus and transovarial transmission has been shown to occur in this species, meaning that infection can be transmitted directly from parent tick to its offspring. Haemaphysalis intermedia is the main tick vector of Ganjam virus in India and Sri Lanka but it has also been isolated from H. wellingtoni, H. parvi, H. rephiciphalus and R. haemophysaloides5. Transstadial transmission (where the pathogen remains in the tick vector across life stages) can occur in all of the host ticks. NSD virus is sensitive to lipid solvents and detergents and is rapidly inactivated at high and low pH. It survives for short periods outside the body—its half-life in serum is reported to be 1.5 hours at 37°C and 7 days at 0°C.
The survival, activity and spread of competent tick vectors plays an important role in spread of the virus. Three major factors have been identified as affecting the transmission and infection intensity of tick-borne diseases worldwide. These are climate change, changes in land use, and movement of animals through importation of livestock or migration of wildlife6. Changes in land use such as agricultural encroachment, wetland modifications and expansion of urban environments have all increased exposure of humans and animals to ticks.
Clinical disease
The incubation period for NSD is 1–15 days but most infections become apparent in 2–6 days. Disease is characterised by acute haemorrhagic gastroenteritis, often beginning with fever, leukopaenia, rapid respiration, anorexia and profound depression. The faeces start as thin, profuse and watery diarrhoea, followed by blood and mucous. The superficial prescapular and subiliac lymph nodes are often palpable and there may be a bloodstained nasal discharge. Pregnant animals often abort. Many animals die within the early febrile stage but deaths are also seen later from diarrhoea and dehydration.
In endemic areas, sheep and goats are often immune to the disease but outbreaks can still occur. This may happen when susceptible, naïve animals are moved into an area where the disease is present and tick vectors are abundant. Outbreaks may also occur when tick populations temporarily or permanently expand their range during periods of high rainfall and other ecological changes.
Disease in humans is rare. The only reported cases have been Ganjam virus infection of laboratory workers in India. The symptoms included fever, abdominal pain and nausea. There has not been any reports of NSD virus in humans.
Diagnosis and treatment
NSD virus can be isolated from uncoagulated blood (plasma) taken from live animals during the initial febrile stage. However, little or no virus can be found in the blood after the body temperature returns to normal.
The most obvious post mortem lesions are congestion and haemorrhage of the gastrointestinal tract, most often in the caecum and colon, appearing as longitudinal striations in the mucosa. The spleen is often enlarged. Virus can be recovered from spleen, lung and mesenteric lymph node tissues.
Laboratory testing is necessary for a definitive diagnosis. RT-PCR or immunofluorescence can be used to detect viral antigens in cell cultures inoculated with suspensions of infected organs, whole blood or serum. The OIE recommends indirect immunofluorescence as the most suitable diagnostic assay. ELISAs can be used but cross reactions with other nairoviruses may occur.
Differential diagnoses include Rift Valley fever, anthrax, heartwater, other causes of haemorrhagic diarrhoea (salmonellosis and coccidiosis), peste des petits ruminants and plant poisoning.
There is no treatment for NSD apart from supportive therapy and in animals with clinical signs the prognosis is poor. While some animals may recover, mortality is usually 30–90 percent during an outbreak.
Prevention and control
There is no commercial vaccine for NSD. However, in endemic countries, experimental vaccines have been developed for use in naïve animals entering enzootic areas, or to protect animals when tick vectors expand their geographical range. No vaccine would be available for use in Australia if the disease occurred here. Control measures in Australia could include movement controls, quarantine, culling of sick animals combined with tick control and acaricide treatment of at risk animals. However, NSD virus has been reported to persist in an infected tick for more than two years, suggesting eradication would be difficult if the disease became established in tick vectors.
Risk to Australia
The main entry pathways into Australia for NSD virus would be legal or illegal importation of infected sheep or goats and the movement of infected ticks. Australia prohibits the import of livestock from regions that have NSD virus or Ganjam virus but tick vectors may be carried unwittingly on goods, other animals and/or people.
NSD has been considered a lower risk disease for Australia than other exotic diseases such as foot-and-mouth disease. However, the global distribution is changing, and it is possible that climate change could lead to the expansion of areas where infection is present. Therefore the risk of disease entering Australia in an infected tick may increase.
Furthermore, NSD viral RNA has been isolated from the tick Haemaphysalis longicornis overseas. This tick is present in southern coastal Queensland, coastal NSW and north-eastern Victoria, and could act as a vector of the disease if it entered Australia.
The identification of NSD virus in new regions and the increasing range of tick vectors that have been shown to carry NSD virus, including H. longicornis which is present in Australia, suggests that NSD may present a greater risk than previously thought.
If an outbreak of NSD occurred in Australia, the economic impact would be significant due to high mortality in sheep and goats, trade and production losses, and the cost of control and eradication. Australia’s response policy is to eradicate NSD in the shortest possible time. However, if NSD virus became established in tick vectors, eradication may not be feasible.
Therefore, prevention and early detection are vital, and veterinarians have an important role to play in early detection of the disease. NSD is a nationally notifiable animal disease and any suspected detection must be reported to state or territory veterinary authorities. The Emergency Animal Disease Hotline can also be contacted on 1800 675 888.
Sally Thomson
Animal Health Policy Branch
Internet resources
The Center for Food Security and Public Health
United States Animal Health Association Foreign Animal Diseases
OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2017
References
1 Lasecka L, Baron MD. The molecular biology of nairoviruses, an emerging group of tick-borne arboviruses. Archives of Virology 2014;159:1249-1265.
2 Yadav PD, Vincent MJ, Khristova M et al. Genomic analysis reveals Nairobi sheep disease virus to be highly diverse and present in both Africa, and in India in the form of the Ganjam virus variant. Infection Genetics and Evolution 2011;11:1111-1120.
3 Perera LP, Peiris JSM, Weilgama DJ, Calisher CH, Shope RE. Nairobi sheep disease virus isolated from Haemaphysalis intermedia ticks collected in Sri Lanka. Annals of Tropical Medicine and Parasitology 1996;90:91-93.
4 Gong S, He B, Wang Z et al. Nairobi sheep disease virus RNA in ixodid ticks, China, 2013. Emerging infectious diseases 2015;21:718-720.
5 Horne KM, Vanlandingham DL. Bunyavirus-vector interactions. Viruses 2014;6:4373-4397.
6 Mohammed K, Tukur SM, Watanabe M et al. Factors influencing the prevalence and distribution of ticks and tick-borne pathogens among domestic animals in Malaysia. Pertanika Journal of Scholarly Research Reviews 2016;2:12-22.