Lumpy Skin Disease: Clinical Picture, Prevention and Control

Editor's Notes

• #2: Lumpy skin disease is also referred to as pseudourticaria, neethling virus disease, exanthema nodularis bovis, and knopvelsiekte.
• #3: Lumpy skin disease is a vector-borne pox disease of domestic cattle and Asian water buffalo and is characterized by the appearance of skin nodules. Lumpy skin disease is classified as a TAD due to its significant economic impact on production and local livelihoods, and to the international trade restrictions it entails in affected countries. In addition, LSD can rapidly spread across national borders and reach epidemic proportions, thus requiring regional cooperation in prevention, control and eradication (OIE, 2016).
• #4: CAUSATIVE AGENT Lumpy skin disease is caused by the lumpy skin disease virus (LSDV), a member of the genus Capripoxvirus (CaPV) within the family Poxviridae. Lumpy skin disease virus shares the genus with sheep pox virus (SPPV) and goat pox virus (GTPV), which are closely related, but phylogenetically distinct. There is only one serological type of LSDV, and LSD, SPP and GTP viruses cross-react serologically. The large, double-stranded DNA virus is very stable, and very little genetic variability occurs. Therefore, for LSDV, farm-to-farm spread cannot be followed by sequencing the virus isolates, as is done with other TADs, e.g. foot-and-mouth disease (FMD).
• #5: Lumpy skin disease is host-specific, causing natural infection in cattle and Asian water buffalo (Bubalus bubalis), although the morbidity rate is significantly lower in buffalo (1.6 percent) than in cattle (30.8 percent) (El-Nahas et al., 2011). Clinical signs of LSD have been demonstrated after experimental infection in impala (Aepyceros melampus) and giraffe (Giraffa camelopardalis). The disease has also been reported in an Arabian oryx (Oryx leucoryx) and springbok (Antidorcas marsupialis). The susceptibility of wild ruminants or their possible role in the epidemiology of LSD is not known. Lumpy skin disease does not affect humans. El-Nahas et al., 2011. Isolation and Identification of Lumpy Skin Disease Virus from Naturally Infected Buffaloes at Kaluobia, Egypt. Global Veterinaria 7 (3): 234-237.
• #6: Lacrimation and nasal discharge are usually observed before other clinical signs As the disease progresses, the nasal discharge becomes mucopurulent
• #7: Subscapular and prefemoral lymph nodes become enlarged and are easily palpable
• #8: High fever (>105oF) usually precedes the appearance of skin lesions and accompanied by a sharp drop in milk yield
• #9: Mild clinical cases may show only a few nodules In severe cases the entire body may be covered with skin lesions Deep nodules involve all layers of the skin, subcutaneous tissue and sometimes even the underlying muscles
• #11: Necrotic plaques in the mucous membranes of the oral and nasal cavities are present Purulent or mucopurulent nasal discharge and excessive salivation, containing high concentrations of virus
• #12: Lesions may occur on the mucous membranes of the eye, accompanied by mucopurulent discharge Painful ulcerative lesions may also in the cornea of one or both eyes, leading to blindness in worst cases
• #13: The clinical signs of LSD vary significantly between animals, with some severely affected and others only mildly affected Silent or subclinical infection can occur, which may complicate control and eradication measures Experimentally, one third of infected cattle do not show any clinical signs, although all become viremic Annandale et al. 2013; Osuagwuh et al. 2007
• #22: Post mortem lesions can be extensive. Characteristic deep nodules are found in the skin which penetrate into the subcutaneous tissues and muscle with congestion, hemorrhage, and edema. Lesions may also be found in the mucous membranes of the oral and nasal cavities as well as the gastrointestinal tract, lungs, testicles, and urinary bladder. Bronchopneumonia may be present, and enlarged superficial lymph nodes are common. Synovitis and tenosynovitis may be seen with fibrin in the synovial fluid. The top photo shows lesions in the oral cavity; the lower photo is a sitfast. (Photos: USDA-APHIS)
• #24: Differential diagnoses include pseudo-lumpy skin disease (a much milder disease caused by a herpesvirus), bovine herpes mammillitis (a disease with lesions generally confined to the teats and udder), dermatophilosis, ringworm, insect or tick bites, besnoitiosis, demodicosis, Hypoderma bovis infestation, photosensitization, bovine papular stomatitis, urticaria, cutaneous tuberculosis, and onchocercosis.
• #26: All samples that have not yet been tested should be considered infected and handledaccordingly. Animals presenting a mild case of the disease do not usually have internal lesions, and there is no need to open severely diseased animals as their external lesions are so obvious. • Scabs are excellent sample material as they are easy to collect, do not require sedation of the animal or local anaesthesia, survive long transport well in different temperatures and contain high concentrations of virus. Collect sufficient volumes of blood: a minimum of 4 ml of vacutainer EDTA (purple top) is needed for PCR testing (note: heparin may hamper the PCR reaction) A. Blood, saliva swabs and tissue samples should be kept at 2-6 °C if the shipment is to last less than 48 hours and at -20 °C if it takes more than 48 hours. B. Serum samples. If transport takes less than five days, the samples can be kept at 2-8 °C degrees in a refrigerator. If more than five days, the clot should be removed and samples stored at -20 °C degrees.
• #28: Several highly sensitive, well-validated, real-time and gel-based PCR methods are available and widely used to detect the presence of CaPV DNA, e.g. Bowden et al., 2008; Stubbs et al., 2012; Ireland & Binepal, 1998; Haegeman et al., 2013; Tuppurainen et al., 2005; Balinsky et al., 2008. These molecular assays cannot differentiate between LSDV, SPPV and GTPV, nor do they indicate whether or not the virus is still infectious. In general, performance of these tests is excellent. Electron microscopy examination can also be used for primary diagnostics although it is uncommon. Live virus can be isolated using various cell cultures of bovine or ovine origin.
• #29: In general, the immune status of a previously infected or vaccinated animal cannot be directly related to serum levels of neutralizing antibodies. Seronegative animals may have been infected at some point and antibody levels do not always rise in all vaccinated animals. The levels of neutralizing antibodies start to rise approximately one week after detection of clinical signs, and affected animals reach the highest antibody levels approximately two to three weeks later. The antibody levels then begin to decrease, eventually dropping below detectable amounts. During ongoing outbreaks, most of the infected animals seroconvert and serum samples can be tested using serum/virus neutralization, immunoperoxidase monolayer assay (IPMA) (Haegeman et al., 2015) or indirect fluorescent antibody test (IFAT) (Gari et al., 2008). It is highly likely that an LSD ELISA will also become commercially available soon. During the inter-epizootic periods (i.e. the quiet periods/years between epidemics
• #30: LSD Preparedness: raising awareness In countries which are at risk of incursion, raising awareness is a critical step in early detection of the disease. Passive surveillance relies on the capability of producers, veterinarian and livestock industry stakeholders to recognize the clinical signs of LSD At a higher level, awareness helps decision-makers to evaluate the severity of the situation and to understand the key measures for disease control and eradication Awareness campaigns should provide all essential information in a simple and easily understandable format to the target audience. Traditional tools such as leaflets, training courses, or meetings are needed, but in case of an emergency, TV, radio, press releases and a wide range of social media channels may reach the target audience faster.
• #31: TARGET AUDIENCE FOR AWARENESS CAMPAIGNS Awareness campaigns should be targeted at official and private veterinarians, both field and abattoir, veterinary students, farmers, herdsmen, cattle traders, cattle truck drivers and artificial inseminators Cattle truck drivers are in a particularly good position to identify infected animals on farms and in slaughterhouses and at cattle collection and resting stations, and to notify veterinary authorities of any clinical suspicion as soon as possible.
• #32: Reporting an outbreak The detection of LSD should be followed by official reporting and initiation of control measures as described in a country’s contingency plan.
• #33: LSD is classified as a notifiable disease by the OIE 1. LSD suspicion at a holding must be reported without delay to the official veterinarian who initiates the disease investigation via official routes Roles, responsibilities and measures to be conducted in response to an LSD outbreak should be described in the country's contingency plan and operational manual . We will discuss some of the key control measures in the next slides 4. Samples are collected for laboratory confirmation by a national or international reference laboratory 5. After the presence of LSD has been confirmed, outbreaks must be reported to the international community via appropriate route, including to an official notification to OIE 6. Essential outbreak data should be shared with neighboring countries at risk
• #34: SURVEILLANCE PROGRAMMES Surveillance programs are based on active and passive clinical surveillance and laboratory testing of blood samples, nasal swabs, or skin biopsies collected from suspected cases. As there are no DIVA vaccines against LSD, serological surveillance is of no use in affected countries or zones where the entire cattle population is vaccinated. However, serology can be used whenever the presence of unnoticed/unreported outbreaks are investigated in disease-free regions either bordering, or in close proximity to, affected regions with unvaccinated cattle. In such regions, the presence of seropositive animals can be considered as an indication of recent outbreaks.
• #35: Control of cattle movement When movement restrictions are implemented, it is important to keep the disruption for farmer’s everyday life and livelihood as low and short-acting as possible Movements of unvaccinated cattle represent the major risk factor for disease spread. During an LSD outbreak, movements of cattle should be strictly regulated, but in practice effective control is often difficult. As a general rule, non-vaccinated animals must not be permitted to move and vaccinated animals should move after full protection has been established by the vaccine, 3-4 weeks post-vaccination. Until sufficient herd immunity has been achieved, the only way to effectively limit the spread of the disease is culling of infected animals and banning cattle movement. Due to vector transmission, restricting movements within an epidemiological unit is not effective. Movements of vaccinated animals can be allowed within a restricted zone within a country after it has been established that full immunity has been provided by a vaccine with proven efficacy (28 days after vaccination). Where nomadic and seasonal farming is practiced, cattle should be vaccinated at least 28 days before going on the move. Movements of unvaccinated breeding animals should not be allowed during outbreaks. Slaughter of cattle should be allowed only in slaughterhouses located within restricted zones because open transport vehicles waiting at their destination may give blood-feeding, flying vectors sufficient time to transmit the virus.
• #36: Vaccination The best protection comes from prophylactic vaccination of the entire cattle population, carried out well in advance in at-risk areas. Only live vaccines are currently available against LSDV. No Differentiation of Infected from Vaccinated Animals (DIVA) vaccines have been developed against LSD. Live vaccines are authorized for use in cattle in Africa, but in other currently affected regions specific authorization is required prior to their use. Annual vaccination is recommended in affected countries, and harmonized vaccination campaigns across regions provide the best protection. Calves from naïve mothers should be vaccinated at any age, while calves from vaccinated or naturally infected mothers should be vaccinated at 3-6 months of age. Homologous Neethling strain-based vaccines provide good protection. Only health animals should be vaccinated with live vaccine. Some side term effects may occur particularly when cattle are vaccinated for the first time. Heterologous vaccines (i.e. sheep pox and goat pox vaccines) can be used if the protection provided by the vaccines has been demonstrated. Heterologous vaccines rarely cause any side effects. Live, attenuated LSDV vaccines may cause mild adverse reactions in cattle. Local reaction at the vaccination site (Fig. 32) is common and acceptable as it shows that the attenuated vaccine virus is replicating and producing good protection Attenuated LSDV vaccines Currently, there are three vaccine producers manufacturing attenuated LSDV vaccines. Live, attenuated LSDV vaccines provide good protection in cattle if 80 percent vaccination coverage is attained. In practice, all animals need to be vaccinated, including small calves and pregnant cows. Regional vaccination campaigns should be preferred to ring vaccination. Attenuated SPPV vaccines Sheep pox virus vaccines have been used in cattle against LSDV in those regions where LSD and SPP are both present. As the protection provided by SPPV vaccines against LSDV is believed to be partial, selection of the vaccine should always be based on demonstrated efficacy of the vaccine against LSDV by a challenge trial carried out in a controlled environment. Attenuated Gorgan GTPV vaccine Commercially available GTPV Gorgan strain has been demonstrated to provide equal protection against LSD as the LSDV vaccines (Gari et al., 2015). Gorgan GTPV vaccine is a good, cost-effective alternative in those countries where GTP and LSD overlap.
• #37: Cattle should be treated regularly with insect repellents to minimize the risk of vector transmission of the disease This measure cannot fully prevent transmission but may reduce the risk. Insect control on animals and in the environment Efficient insect control on cattle or in holdings may reduce the rate of mechanical transmission, but cannot totally prevent it, particularly where cattle are free-roaming or kept in fenced pastures Anti-mosquito nets can be considered in cases when cattle are permanently kept indoors. The application of spot-on repellents can protect cattle from insects and ticks for short periods. When insecticides are used, withdrawal times for milk and meat need to be considered. Large-scale use of insecticides in the environment is not recommended as it may be harmful to the ecological balance, and to other useful insects such as honeybees. Moreover, the risk to the environment is not fully understood. Limiting vector breeding sites such as standing water sources, slurry and manure, and improving drainage in holdings are sustainable, affordable and environmentally friendly ways of reducing the number of vectors on and around cattle.
• #38: Cleaning and disinfection of personnel, premises, and the environment Lumpy skin disease virus is very stable and survives well in extremely cold and dry environments within the pH range 6.3-8.3. Infected animals shed scabs from skin lesions. Inside the scabs, the virus may remain infectious for several months. Thorough cleaning and disinfection with appropriate products should be performed on affected farms, trucks, premises and potentially contaminated environments. Personnel should also undergo disinfection. Although LSDV is sensitive to most disinfectants and detergents, in order to effectively decontaminate animal facilities and holdings, mechanical removal of surface material such as dirt, manure, hay and straw is required beforehand. The disinfectant selected must be able to penetrate any organic material surrounding the infectious virus in the environment. FAO provides practical recommendations for decontamination of premises, equipment and the environment in the Animal Health Manual on Procedures for Disease Eradication by Stamping Out (FAO, 2001). Susceptible to ether (20%), chloroform, formalin (1%), and some detergents, e.g. sodium dodecyl sulphate. Susceptible to phenol (2%/15 minutes), sodium hypochlorite (2–3%), iodine compounds (1:33 dilution), Virkon® (2%), quarternary ammonium compounds (0.5%).
• #39: Biosecurity measures at holdings In the event of LSD entering a country, farm biosecurity should be raised to the highest feasible level, taking into consideration the limits of the epidemiological unit in each case. As the disease is spread by vectors, such measures may not totally prevent an incursion, but the risk can be reduced. Purchase of new animals that are either incubating the disease or are viremic without exhibiting any symptoms presents a major risk of introducing the disease into a naïve herd. Introduction of new animals into herds should therefore be limited. Stock should be bought only from trusted sources. New animals should be examined and declared free of clinical signs prior to movement and on arrival, and should be kept separated/quarantined from the herd for at least 28 days. Farm visits should be restricted to essential services with entry points to properties limited. All visitor vehicles and equipment should be cleaned in a wash-down bay when entering farms. Boots should also be cleaned or, alternatively, shoe covers should be worn. Visitors entering farms should wear clean protective clothing.
• #40: Stamping out policy A total stamping out policy may not be feasible, affordable or acceptable in all countries due to limited resources or for cultural reasons. Those animals that show clinical signs should always be removed from the herd because the viremic animals with skin lesions serve as a source of virus for the others. The severely infected animals may not regain their pre-infection production level. An EFSA study conducted in 2016 suggested that if the vaccination coverage is 80% or more, then there is no major difference between total and partial stamping out (i.e. culling of affected animals) in terms of the probability of eradicating infection. Disposal of large number of carcasses may be an environmental problem and a logistical challenge. According to the EFSA urgent advice on lumpy skin disease, vaccination has a greater impact in reducing LSDV spread than any stamping-out policy (EFSA, 2016). As an example, EU member states are bound by EC Directive 92/119/EEC which sets out measures to be conducted in response to an LSD outbreak, including census of animals, restriction of movement, culling of animals, and the safe disposal of animals, products and by-products. It also includes measures regarding an epidemiological inquiry, vector control, cleaning and disinfection. Stamping out policy When a stamping-out policy is implemented, culling and disposal of carcasses should take place as soon as possible in compliance with all animal welfare and safety requirements. Disposal by burial or burning should follow national rules on environmental protection. In some countries, these practices may not be allowed at all. Appropriate methods for culling cattle are premedication and injection with barbiturates or other drugs, followed by captive-bolt stunning and pithing or free bullet Disposal of carcasses should be conducted by burial, burning or rendering, according to national procedures. Importantly, regardless of the stamping-out policy selected, severely affected animals should always be removed from the herd because they serve as a constant source of contamination for biting and blood-feeding vectors. In the same way, no animal showing any clinical signs of LSD should be sent to a slaughterhouse, but should be culled and disposed of either on-site or at an appropriate rendering plant
• #41: Stamping out policy: compensation A compensation policy is highly recommended. If compensation is not available, there is likely to be underreporting of disease and further spread. Compensation may be either full or partial market values. If farmers are allowed to send their animals for slaughter house then compensation may cover the difference between market value and price of the meat. Compensation may also involve replacing a dead or culled animal with a vaccinated animal. If only those cattle that have been died from LSD are compensated, then euthanasia of affected sick animals may not be carried out, potentially leading to prolonged suffering and major animal welfare issue