Lumpy Skin Disease
Lumpy skin disease (LSD) is a contagious vector-borne disease that affects cattle (Bos taurus and Bos indicus) and Asian water buffalo (Bubalus bubalis) and significantly impacts production, resulting insubstantial economic losses. The transboundary disease is notifiable to the World Organization Animal Health (1).
LSD is caused by the lumpy skin disease virus (LSDV) which belongs to the Capripoxvirus genus within the Poxviridae family. LSDV is closely related antigenically to two other Capripoxvirus, Sheeppox virus and Goatpox virus, which makes the three viruses difficult to discriminate using routine serological tests. Diagnostic methods rely on detecting the virus, for example by PCR or virus isolation. The name of the disease originates from the clinical presentation, which is generally associated with the appearance of skin nodules that may cover the entire body of the animal during severe infection. While mortality rates in cattle are often low (between 10-20% (2)), the relatively high morbidity of LSD once introduced into naïve populations can lead to significant income losses for farmers from decreased milk production, damaged hides, emaciation of animals, infertility and abortions (3). Animals recover from LSD and are not known to carry the virus following their recovery.
Transmission of LSD is facilitated by a broad range of insects, from lice to mosquitoes. As vector numbers increase with favorable environmental conditions such as hot and humid weather and wetlands, so is the occurrence of LSD (4). LSDV can also be transmitted via close contact with infected animals and shared water sources or grazing pastures (4). The detection of LSDV in wild ruminants in Africa and Asia are suggests wildlife could be a reservoir of LSDV, but further evidence is still needed (4–6).
In recent years, LSDV has extended its geographical range from the endemic sub-Saharan area to the Middle East, Russia and Asia making it a transboundary disease. Since 2019, LSD outbreaks have been reported in Asian countries, and the disease has now spread across the region, including Southeast Asia (7). This is particularly concerning given that the world’s largest cattle populations are found in Asia (3). Since LSD was first described and recorded in Zambia in 1929, LSD outbreaks have been notified to WOAH in eighty countries worldwide. Twenty-five of them reported the disease’s first occurrence in 2023 and 2024 (8, 9). LSD’s fast range expansion has raised concerns about the potential introduction of the virus into LSD-free countries with large, naïve cattle populations, such as Australia (10).
LSD in Europe
LSD became a serious threat in Europe after reoccurrence of the disease was reported in Israel (2012), Turkey (2013), Azerbaijan (July 2014) and Russia (July 2015). In August 2015, LSD was notified for the first time by a European Union country: outbreaks were reported in the Northeastern part of Greece at the border with Turkey (11). The disease continued to spread in neighboring countries through 2016: thousands of outbreaks were recorded in Albania, Bulgaria, Greece, Kosovo, Montenegro, North Macedonia and Serbia (12). The disease spread was found to be favored by the proximity between infected farms, and an abundance of associated vectors (13).
To limit the spread and impact of LSD, a coordinated multinational mass vaccination campaign with live attenuated LSD vaccine was launched in 2016 and continued until 2019 in South-Eastern Europe: millions of cattle were vaccinated during that period, which helped contain the spread. By 2018, there were no more outbreaks except in Turkey, which reported its last LSD outbreak in 2021 (13). Countries in that region implemented both passive and active surveillance programs to regain disease freedom (with vaccination).
One of the key aspects for the successful control of the LSD outbreaks in that part of Europe was the joint effort between veterinary authorities of all Balkan countries transboundary coordinated by the European Commission from 2015 to 2017 (14). Sustainable eradication of LSD however is an enormous challenge in countries that are neighboring LSD-infected regions (14) .
LSD in Africa and Middle East
After the first occurrence of LSD in Zambia in 1929, the disease soon became endemic in several regions of sub-Saharan Africa. Zimbabwe in particular presents some of the highest incidence of LSD outbreaks in the region (9). Factors contributing to these outbreaks included animals sharing grazing and drinking sites, presence of a vector population, improper vaccinations, and the introduction of new animals on farms (9). At present, Algeria, Morocco and Tunisia are the only countries in Africa where LSD has not been reported (15). However, Libya reported its first cases of LSD on cattle farms in the northwestern part of the country last year (2023). The proximity of the outbreaks to Tunisia’s eastern border is a cause for concern as LSD could potentially spread across the Maghreb region via vector or live animal movements (16).
In the Middle East countries, LSD has been reported since the late 1980s, especially in Egypt and Israel. Outbreaks have been associated with highly humid and warm conditions and possibly with stable flies as vectors. In the 1990s further cross-boundary transmission led to LSD progressing across the Arabic Peninsula with outbreaks reported in Kuwait, Lebanon, Yemen, the United Arab Emirates, Bahrain, Oman, Jordan, Iraq, Iran, Syria, Azerbaijan, and Kazakhstan (17). In these countries, LSD was primarily considered an epizootic disease as the local populations of arthropod vectors were low. The introduction was likely to be associated with clinically sick animals being moved illegally or with movements of asymptomatic infected animals and vectors. According to WOAH’s WAHIS database LSD is currently present in the majority of the Middle East (8).
LSD in Asia
In 2019, LSD spread further East towards Asia, with reports of outbreaks in Pakistan, Kazakhstan, Russia, China, India, Bangladesh, and Nepal (18). LSD was first reported in Southeast Asia in October 2020 in Vietnam (Huu Lung District, Lang Son Province). Between 2020 and 2023, the disease extended to Cambodia, Laos, Malaysia, Myanmar, Thailand, Indonesia and Bhutan (19). In October 2023, LSD was identified for the first time in South Korea (19)
The recent LSD introductions and spread across Asia are a major concern, as the detection of this exotic disease may have severe trade implications for infected countries. Asia is a major pillar for cattle and buffalo production globally, being home to more than 650 million head of cattle and buffaloes, or 39 percent of the global stock (20). India has the largest number with nearly 300 million head, followed, albeit distantly, by China (approximately 90 million), and Pakistan (approximately 85 million) (20). India is also the second largest beef exporter worldwide. The economic impact of LSD on South, East and Southeast countries in Asia was estimated to be up to USD 1.45 billion in direct losses of livestock and production (20).
Vaccination – a challenge
LSD control is achieved using a combination of strategies, including vaccinating more than 80 percent of the susceptible population, which is a core aspect for control (19). The spread of the disease cannot be controlled effectively and sustainably without the use of vaccination (21).
Currently, most commercially-available vaccines against LSD are live attenuated vaccines using either a LSDV strain, a Sheeppox virus, or Goatpox virus (14). The main difference between the vaccines is their level of attenuation which influences the immune response, side effects, dosage and therefore cost of a vaccine dose. As a consequence, the attributes of the live attenuated vaccines for LSD available vary considerably (14, 21). The development of protective immunity takes approximately two to three weeks post-vaccination according to the manufacturers. Reversable clinical signs of LSD such as fever, decrease in milk production or sometimes nodules at the skin, have been reported as adverse effects of live attenuated vaccines (22). As there are no DIVA (Differentiating Infected from Vaccinated Animals) vaccines commercially available for LSDV, it is not possible to differentiate between vaccinated and naturally infected animals based on serology in a region or country where live attenuated vaccines are used. This is a significant problem to set up surveillance programs if serology cannot be used. DIVA PCR tests are available but should not be relied on when recombinant viral strains are circulating. Inactivated vaccines for LSD have been recently developed but they provide a shorter protection period against LSDV, requiring more frequent vaccination of animals, which has both practical and economic consequences (14). Inactivated vaccines present significant advantages in countries free of LSD but under pressure from neighboring infected countries.
Selecting and accessing suitable LSD vaccines can be a challenge for farmers and veterinary authorities in many countries. When the disease occurs for the first time in a country, authorities are often facing delays in obtaining supplies due to the ongoing high international demand for quality vaccines. The strict storage and use conditions for live attenuated vaccines (use within six hours after reconstitution under 8 °C in the shade) are difficult to achieve in field settings for some regions. Another challenge described is the lack of affordability of vaccines especially for developing countries. For example, in many LSD-endemic African countries, the government does not provide financial support to cover the LSD vaccines and vaccination, mainly because LSD is not seen as a high-priority disease due to the low mortality and morbidity rates in endemic settings. The vaccination costs are therefore covered by farmers themselves (14).
LSD vaccination strategies vary greatly around the globe. This is mainly due to the different epidemiological settings but also because of variations in national and regional policies and in resources availability. In the absence of any organized approaches to control the disease in endemic areas, farmers can only use vaccination as a stand-alone protective measure, which has been common practice over the past decades in sub-Saharan Africa (21,23,24). In local LSD-outbreak scenarios, ring vaccination of cattle and Asian water buffalo populations are applied (22,25). In combination with rigorous movement restrictions, the same approach could succeed to control outbreaks and eradicate the disease locally, as seen in Greece and neighboring countries in the late 2010s. In this case, countries have committed to vaccinating their susceptible populations for several years in a row (14). However, additional emphasis on the disease surveillance programs is required after compulsory vaccination in order to avoid the re-emergence of the disease. For maximum impact, vaccination against LSD should be embedded into existing disease control programs and risk-based surveillance, rather than stunting potential vaccine efficacy by treating it as a stand-alone measure.
However, especially Southeast Asian countries are facing certain challenges which were well described by the FAO (20). For example, despite high cattle and buffalo density in villages and communal sharing of watering and grazing areas with humid and warm conditions; a lack of traceability together with a lack of efficiently regulated livestock production and market chains are identified as issued. Furthermore, knowledge gaps related to LSD epidemiology, vector ecology, efficacy and cost-effectiveness of the different control options, lack of doses of potent and safe LSD vaccines and the logistic and technical capacities for mass vaccination were described. Thus, these aspects need to be addressed for successful control (10).
Outlook on Lumpy Skin Disease
Given LSD’s fast transboundary spread and the challenges associated with vaccination, the emergence of the disease in naïve cattle and buffalo populations is set to continue and threaten large food production markets. Only international coordinated efforts and public-private partnerships will help keep the disease under control and therefore minimize the socio-economic impacts of LSD both regionally and globally.
References
1. Lumpy Skin Disease (LSD) - WOAH - Asia [Internet]. [cited 2024 Feb 13]. Available from: http://rr-asia.woah.org/en/projects/lumpy-skin-disease-lsd/
2. LUMPY SKIN DISEASE Aetiology Epidemiology Diagnosis Prevention and Control References. [cited 2024 Feb 19]; lumpy-skin-disease.pdf (woah.org)
3. Introduction and spread of lumpy skin disease in South, East and Southeast Asia Qualitative risk assessment and management Introduction and spread of lumpy skin disease in South, East and Southeast Asia. [cited 2024 Feb 7]; Available from: https://doi.org/10.4060/cb1892en
4. Bianchini J, Simons X, Humblet MF, Saegerman C. Lumpy Skin Disease: A Systematic Review of Mode of Transmission, Risk of Emergence and Risk Entry Pathway. Viruses [Internet]. 2023 Aug 1 [cited 2024 Feb 19];15(8). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10458895/
5. Kara A;, Last P;, Romito RD;, Wallace M;, Haegeman A, Van Schalkwyk A, et al. Detection and Genome Sequencing of Lumpy Skin Disease Viruses in Wildlife Game Species in South Africa. Viruses 2024, Vol 16, Page 172 [Internet]. 2024 Jan 24[cited 2024 Feb 13];16(2):172. Available from: https://www.mdpi.com/1999-4915/16/2/172/htm
6. Porco A, Chea S, Sours S, Nou V, Groenenberg M, Agger C, et al. Case report: Lumpy skin disease in an endangered wild banteng (Bos javanicus) and initiation of a vaccination campaign in domestic livestock in Cambodia. Front Vet Sci. 2023 Aug3;10:1228505.
7. Azeem S, Sharma B, Shabir S, Akbar H, Venter E. Lumpy skin disease is expanding its geographic range: A challenge for Asian livestock management and food security. The Veterinary Journal. 2022 Jan 1;279:105785.
8. WAHIS [Internet]. [cited 2024 Feb 13]. Available from: https://wahis.woah.org/#/dashboards/country-or-disease-dashboard
9. Anwar A, Na-Lampang K, Preyavichyapugdee N, Punyapornwithaya V. Lumpy Skin Disease Outbreaks in Africa, Europe, and Asia (2005–2022): Multiple Change Point Analysis and Time Series Forecast. Viruses [Internet]. 2022 Oct 1 [cited 2024 Feb 12];14(10):2203. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9611638/
10. Lumpy skin disease - DAFF [Internet]. [cited 2024 Feb 7]. Available from: https://www.agriculture.gov.au/biosecurity-trade/pests-diseases-weeds/animal/lumpy-skin-disease
11. Tasioudi KE, Antoniou SE, Iliadou P, Sachpatzidis A, Plevraki E, Agianniotaki EI, et al. Emergence of Lumpy Skin Disease in Greece, 2015. Transbound Emerg Dis[Internet]. 2016 Jun 1 [cited 2024 Feb 8];63(3):260–5. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/tbed.12497
12. Tuppurainen ESM, Antoniou SE, Tsiamadis E, Topkaridou M, Labus T, Debeljak Z, et al. Field observations and experiences gained from the implementation of control measures against lumpy skin disease in South-East Europe between 2015 and 2017. Prev Vet Med. 2020 Aug 1;181:104600.
13. Lumpy skin disease: I. Data collection and analysis. EFSA J [Internet]. 2017 Apr 22 [cited 2024 Feb 12];15(4). Available from: https://pubmed.ncbi.nlm.nih.gov/32625471/
14. Tuppurainen E, Dietze K, Wolff J, Bergmann H, Beltran‐alcrudo D, Fahrion A, et al. Review: Vaccines and vaccination against lumpy skin disease. Vaccines (Basel). 2021 Oct1;9(10).
15. Eom HJ, Lee ES, Yoo HS. Lumpy skin disease as an emerging infectious disease. J Vet Sci [Internet]. 2023 [cited 2024 Feb 12];24(3). Available from: https://europepmc.org/article/PMC/PMC10244130
16. PreliminaryOutbreak Assessment Lumpy Skin Disease in Libya Disease report. 2023 [cited 2024 Feb 12]; Available from: https://lywitness.com/60576/%d8%a7%d9%84%d8%ac%d9%84%d8%af-
17. Akther M, Akter SH, Sarker S, Aleri JW, Annandale H, Abraham S, et al. Global Burden of Lumpy Skin Disease, Outbreaks, and Future Challenges. Viruses [Internet]. 2023 Sep 1 [cited 2024 Feb 13];15(9). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10535115/
18. Wilhelm L, Ward MP. The Spread of Lumpy Skin Disease Virus across Southeast Asia: Insights from Surveillance. Transbound Emerg Dis. 2023;2023.
19. Preliminary Outbreak Assessment Lumpy Skin Disease in East Asia. 2023;
20. Introduction and spread of lumpy skin disease in South, East and Southeast Asia Qualitative risk assessment and management Introduction and spread of lumpy skin disease in South, East and Southeast Asia. [cited 2024 Feb 12]; Available from: https://doi.org/10.4060/cb1892en
21. Whittle L, Chapman R, Williamson AL. Lumpy Skin Disease—An Emerging Cattle Disease in Europe and Asia. Vaccines (Basel) [Internet]. 2023 Mar 1 [cited 2024 Feb 13];11(3). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10057024/
22. Calistri P, De Clercq K, Gubbins S, Klement E, Stegeman A, Cortiñas Abrahantes J, et al. Lumpy skin disease epidemiological report IV: data collection and analysis. EFSA Journal. 2020 Feb 1;18(2).
23. Molla W, de Jong MCM, Gari G, Frankena K. Economic impact of lumpy skin disease and cost effectiveness of vaccination for the control of outbreaks in Ethiopia. Prev Vet Med. 2017 Nov 1;147:100–7.
24. Ochwo S, VanderWaal K, Munsey A, Ndekezi C, Mwebe R, Okurut ARA, et al. Spatial and temporal distribution of lumpy skin disease outbreaks in Uganda (2002-2016). BMC Vet Res [Internet]. 2018 Jun 1 [cited 2024 Feb 14];14(1):1–12. Available from: https://bmcvetres.biomedcentral.com/articles/10.1186/s12917-018-1503-3
25. Lumpy skin disease of cattle: A growing problem in Africa and the Near East [Internet]. [cited 2024 Feb 14]. Available from: https://www.fao.org/3/u4900t/u4900T0d.htm
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