Lumpy skin disease: a significant threat to Australia

Keywords: Australia, buffalo, capripoxvirus, cattle, emergency animal disease, lumpy skin disease, poxvirus, South‐East Asia, surveillance, vector.

Lumpy skin disease (LSD) is a severe, vector-borne disease that affects cattle and Asian water buffalo (Bubalus bubalis).¹ All breeds of cattle are susceptible, but both beef and high milk producing Bos taurus animals are more susceptible than Bos indicus breeds. Lumpy skin disease virus (LSDV) is a highly host-specific member of the genus Capripoxvirus, family Poxviridae, and is closely related to sheeppox and goatpox viruses with at least 96% identity at the genome level.^2,3

Lumpy skin disease usually results in medium to high morbidity (2–45%) and low mortality (<10%) in naïve populations and is characterised by the development of multifocal cutaneous skin nodules (up to 5 cm in diameter), pyrexia (fever), lymphadenopathy (enlarged lymph nodes), depression, reduced milk production and permanent hide damage.^1,4 It is notifiable to the World Organisation for Animal Health (WOAH) due to its capacity for rapid transboundary spread and is considered one of the most economically important viral diseases of cattle due to its impacts on animal health, production and trade.^5,6

The Australian Federal Government response to incursion is well documented.^7,8 However, regaining disease free status would require at least 14 months from the detection of the last case of LSD before trade sanctions could be lifted⁹ having significant repercussions for the Australian economy.

Lumpy skin disease is considered endemic to much of Africa and, prior to 2012, detection of this disease outside of endemic areas was largely confined to sporadic outbreaks in the Middle East.^5,10 In the past 10 years, LSDV entered eastern Europe and was successfully controlled only after the implementation of a comprehensive and widespread vaccination program, with LSD remaining endemic in Turkey.¹¹ Lumpy skin disease subsequently spread through India and China and more recently into South-East Asia (WAHIS (woah.org)) with outbreaks reported in Myanmar and Thailand in November 2020 and March 2021, respectively. In contrast to the sporadic and gradual spread of LSD seen historically, spread throughout South-East Asia has occurred more rapidly, with outbreaks in Malaysia (May 2021), Laos (May 2021), Singapore (March 2022) and Indonesia (February 2022) now reported^12,13 (Fig. 1).

Fig. 1.  Global distribution of confirmed lumpy skin disease outbreaks reported to the Food and Agriculture Organization of the United Nations (FAO) EMPRES Global Animal Disease Information System (EMPRES-I; https://empres-i.apps.fao.org/) between January 2018 and November 2022.

The accelerated spread of LSD is most likely associated with significant cross-border animal movement and insect vector activity, however questions about altered virulence characteristics of emerging strains have been raised.¹⁴ Genomic sequencing of the South-East Asian isolates have shown that some of the emerging strains are vaccine-like recombinants which have most likely resulted from suboptimal vaccine manufacturing,¹⁵ but assessment of virulence characteristics have not yet been undertaken. To our knowledge, the strain circulating in Indonesia has not yet been sequenced and so its phylogenetic origin is unknown.

However, when considering the likely routes of incursion of LSD into South-East Asia, it is feasible to expect the virus circulating within Indonesia will be closely related to either the Hong Kong (2020) or Thailand (2021) strains. Sequencing of these strains demonstrate that each is closely related to vaccine strains suggestive of recombination during vaccine manufacture.^16,17 Assessment of the comparative pathogenesis of these variants has not yet been published and so any potential differences in virulence or transmission characteristics are unknown.

The current distribution of LSD within Indonesia is not well understood because early eradication and surveillance efforts have been complicated by the recent detection of foot-and-mouth disease. To date, there have been no cases of LSDV in either Papua New Guinea or Timor-Leste reported to WOAH (WAHIS (woah.org)).

Since Australia does not share land borders with our near-neighbours, and with LSD being a vector-borne disease, natural pathways that facilitate the introduction of infected vectors, rather than introduction of infected animals, are considered the most likely route of incursion into Australia.⁷ As evidenced by the emergence of new bluetongue virus variants, there is precedent for the wind-borne introduction of infected vectors into northern Australia.^18,19 Given the current trajectory of spread through South-East Asia and significant regulated and unregulated movement of animals amongst Indonesia, Papua New Guinea and Timor-Leste, northern Australia is considered most vulnerable.

This presents a major challenge in keeping LSD out of the country. Natural pathways are much more difficult to manage and monitor when compared with regulated pathways (e.g. food products). Further, predicting the most likely point of entry to ensure targeted surveillance efforts hinges on the accuracy of predictive modelling. There are many gaps in our knowledge pertaining to the climatic events and retention of vector competency through such events which generates uncertainty in the risk assessments.

What is known, however, is that outbreaks of LSD are commonly phasic and are associated with climatic conditions which favour insect activity. Typically, outbreaks occur in warm, humid and moist conditions, with transmission decreasing as ambient temperatures drop.¹¹ For South-East Asia and northern Australia, climatic conditions favouring vector activity occur between August and April each year and so the likelihood of continued spread of LSD eastward through Indonesia, in the absence of a comprehensive vaccination program, is high.

Vector flight distance, proximity to susceptible cattle populations and likelihood of surviving long distance wind-dispersal impact risk profiling and modelling for incursion. If introduced, studies have demonstrated that a wide range of biting insects including mosquitoes, midges, biting flies and ticks are capable of mechanically transmitting LSDV, however longevity of virus survival within these vectors is variable.^20–23 Ticks are unlikely to facilitate rapid spread of disease but may act as an environmental reservoir and facilitate overwintering of the virus which could impact eradication efforts.^22–24

The local conditions, numbers of insects, flight distance, feeding behaviour and lifespan determine the importance of individual vector species and will be regionally specific. Australia has a diverse range of potential vectors that could aid in transmission of LSDV if incursion occurs, with some of the vector species of primary concern, given their numbers in northern Australia, being the buffalo fly (Haematobia exigua) and midges (Culicoides species) (flyboss.com.au). The role of midge species in virus uptake and onward transmission is thought to be low, but the importance of buffalo fly has not been determined. The minimal infective dose and, by extrapolation, the number of vectors required to establish infection in cattle is not well established.

Early detection and response to an incursion of LSD in northern Australia would be challenging. There are a significant number of unmanaged feral cattle and buffalo in northern Australia and effective response efforts would be impaired by lack of access to these populations. Further, in naïve populations, detection of acute disease would form the basis of a presumptive diagnosis which, due to the presence of other diseases with similar clinical features in cattle,²⁵ must be confirmed by laboratory diagnosis. However, during the wet season in northern Australia, physical access to managed cattle can be limited and so detection of an index case may be delayed.⁷

It is well recognised that large-scale vaccination of susceptible bovine populations is the most effective means to control and limit the spread of LSD.²⁶ Currently, only live attenuated vaccines are readily available. However, although highly effective, they should be sourced from reputable vaccine manufacturers, be well characterised and shown to be free of adventitious agents before use. For Australia, as for other lumpy skin disease free countries, the pre-emptive use of LSD vaccines would result in the loss of disease-free status and have immediate impacts on trade and, as such, is unlikely to form part of any pre-incursion risk mitigation activities.

Consequently, surveillance and preparedness activities are currently focused on assisting affected near neighbouring countries to control disease outbreaks, further enhancing diagnostic assays used for surveillance activities and contributing to key knowledge gaps of significance to Australia.

Following extensive consultation between the Australian Government, State and Territory Governments, industry and non-governmental stakeholders, a National Lumpy Skin Disease Action Plan has been developed to guide and coordinate these activities.²⁷

If an outbreak of lumpy skin disease were to occur in Australia, particularly in the extensive northern cattle industry, eradication would likely be challenging. There are a broad range of biting insects that would likely be able to transmit the virus within susceptible populations. Further, ticks may play a role in maintenance of the virus for extended periods. Early detection of disease may be hindered by periods of inaccessibility to northern Australian herds, especially during the wet season, and populations of unmanaged cattle and buffalo are likely to complicate eradication efforts.

However, with respect to our near neighbouring countries, LSD is confined to Indonesia with Papua New Guinea and Timor-Leste considered disease free. The reported distribution of disease within Indonesia is, however, based on the initial notification to WOAH and may not be reflective of the current status.

Should LSDV spread into Papua New Guinea and/or Timor-Leste, the most likely route of incursion into Australia would be via wind-dispersal of infected vectors into northern Australia from these countries. Risk modelling, targeted surveillance, development and validation of improved diagnostic tests, and development and assessment of vaccine candidates suitable for use in Australia are key aspects of preparedness.

Data sharing is not applicable since no new data were generated or analysed during this study.

The authors declare no conflicts of interest.

This research did not receive any specific funding.