empres watch VOL 29 November 2013 [email protected] | www.fao.org/ag/empres.html Emergence of lumpy skin disease in the Eastern Mediterranean Basin countries

Contributors: Sherrylin Wainwright a, Ahmed El Idrissi a, Raffaele Mattioli a, Markos Tibbo b, Felix Njeumi a, Eran Raizman a a Food and Agriculture Organization of the (FAO); b FAO Regional Office for the Near East (FAO-RNE)

Animal Health (OIE). considering the area’s substantial livestock Contents LSD was first reported in Africa, where it population. Turkey maintains over 11.3 million crippled the production potential of and heads of cattle. Iraq, Lebanon and the Syrian 1. Introduction 1 compromised vulnerable livelihoods on the Arab Republic maintain 2.8 million heads, continent. LSD moved beyond Africa in 1989 and the Islamic Republic of Iran maintains 2. Risk assessment 3 when Israel confirmed its first LSD outbreak. for approximately 8.5 million heads. Armenia, In subsequent years Bahrain, Kuwait, Oman, Azerbaijan and Georgia combined maintain 3. Risk management Yemen and the West Bank also reported LSD 4million heads. options for at-risk incursion. Lebanon and Jordan joined LSD- At-risk countries include the Russian countries 4 affected countries in 2012 and 2013, and Federation to the north and Bulgaria and most recently Turkey reported the disease in Greece to the west. This is in line with the 4. Conclusions 5 October 2013 (see Table 1). spread of other significant transboundary There is an imminent risk that LSD will animal diseases (e.g. African swine fever, 5. References 5 (or has already) become endemic in some foot-and-mouth disease, sheep pox and goat countries in the Middle East. Although LSD pox) in the region. Moreover, capripoxviruses has not been reported in the Syrian Arab could be considered emerging disease 1. Introduction Republic – most likely due to the current threats because of global climate change and armed conflict – the disease probably alterations to the trade patterns of animals 1.1 Occurrence of lumpy skin travelled through the Syrian Arab Republic to and animal products. 2 disease in Middle East Turkey. LSD may also be in Iraq. Furthermore, umpy skin disease (LSD) is caused the situation raises concerns that the disease 1.2 Epidemiology by the lumpy skin disease may continue spreading: i) north and west The morbidity rate for LSD ranges from 5 to L (i.e. , ). The from Turkey into Europe and the Caucasus; 45 percent depending on the: i) distribution virus mainly affects cattle and Asian and ii) east to Central and South Asia. and abundance of insect vectors; ii) breed water buffaloes. LSD can cause devastating LSD shows significant potential for of cattle affected; and iii) general health and economic impacts. 1 New outbreaks of LSD major socio-economic impacts should it nutritional status of the animals in question. in previously free regions require immediate continue spreading: i) throughout newly Occasional mortality rates from 10 to beyond notification under the Terrestrial Animal affected countries; and ii) into their LSD- 40 percent have been reported, but the rate of Health Code of the World Organisation for free neighbours. This is especially alarming 1 to 5 percent is considered more usual.

Table 1. LSD outbreaks, as reported to OIE*

Countries 2006 2007 2008 2009 2010 2011 2012 2013 Bahrain present present 0 present 0 0 0 0 Egypt present 0 0 0 0 0 present present Israel present present 0 0 0 0 present present Jordan 0 0 0 0 0 0 0 present Lebanon 0 0 0 0 0 0 present present Oman present 0 0 present present present present 0 West Bank present present present 0 0 0 0 present Turkey 0 0 0 0 0 0 0 present

* 0 = country reported zero cases for that year to OIE; present = country reported disease present that year to OIE VOL 29 NOVEMBER 2013 | empres watch

1.3 Transmission 1.5 Diagnosis RM 65 [Jordan Bio industries Centre, JOVAC] and the Tissue Culture Sheep Different types of biting and blood-feeding The manifestation of LSD may range from Pox Vaccine [Kenyan S/GP 0240, arthropods (including mosquitoes and flies3,4) acute to subclinical (see Table 2). VSVRI, Egypt]). are likely responsible for the mechanical 5 1.6 Virus susceptibility spread of the LSD virus . Disease incidence 1.8 Laboratory is highest in wet/warm weather. Incidence Disinfection is possible using ether decreases during the dry season, which is (20 percent), chloroform, formalin (1 percent) When disease is introduced for the first time, possibly linked to decreases in insect vector and some detergents (e.g. sodium dodecyl a fast and accurate laboratory confirmation occurrence/numbers. Minor sources of sulphate; phenol [2 percent/15 minutes], of the tentative field diagnosis is required infection could include direct and indirect sodium hypochlorite [2–3 percent], before beginning relatively expensive control contact (e.g. through infective-saliva iodine compounds [1:33 dilution], Virkon® and eradication measures. Virus isolation contaminated feed and water). Other [2 percent] and quaternary ammonium and molecular diagnostic tests play an potential transmission routes include the milk compounds [0.5 percent]). 12 important role in monitoring the spread of the of lactating cows and the semen of infected capripoxviruses and controlling outbreaks bulls, since the LSD virus can persist for 1.7 Vaccine in susceptible livestock. However, those extended periods of time in both 6,7. Live, attenuated vaccines are commonly used laboratories which are poorly equipped or against LSD. This is because immunity to located in challenging field environments 1.4 Host susceptibility capripoxviruses is mainly cell mediated and is face difficulties accessing these molecular Susceptibility and eventual disease severity better stimulated by the use of live vaccines. techniques that rely upon expensive depends on the dose and route of virus While effective, live vaccines occasionally equipment. inoculation as well as the health and cause serious side effects (e.g. intense The development of a loop-mediated nutritional status of the affected animal. local reaction at the vaccination site, which isothermal amplification (LAMP) assay Considered at risk are all cattle breeds plus rarely develop into generalized infection and for rapid detection of capripoxviruses has Asian water buffaloes (Bos Bubalis). Bos frequently cause a temporary decrease in milk been shown to be highly specific with no taurus cattle breeds are more susceptible production). Due to cell mediated immunity, apparent cross-reactivity to other related than Bos indicus breeds, and young calves low antibody responses are common after (i.e. near neighbours) or viruses that often experience more severe disease than vaccination with attenuated live vaccines, cause similar clinical signs (i.e. look-a-like adults. Although the incubation period under even though vaccinated animals are fully viruses). When compared to highly sensitive field conditions has not been reported, protected. 13 Inactivated vaccines do not quantitative real-time polymerase chain the onset of fever following inoculation is provide long-term immunity; therefore, annual reaction assay (PCR). LAMP and quantitative, in 6–9 days. The first skin lesions appear booster vaccinations are recommended. real-time PCR exhibited similar analytical at the inoculation site in 4–20 days. 8 No Vaccination has shown to reduce the negative sensitivities. Overall agreement on diagnostic carrier status is recognized in cattle following economic impacts of LSD. 14 test results between the two assays was infection with LSD virus. Live virus can be Vaccines used presently in the Middle East 90–95 percent for specificity and 89–100 detected up to 39 days post-infection in the include: percent for sensitivity. The LAMP assay is dried crust of skin lesions on an infected • homologous live attenuated vaccines simple to use, inexpensive, highly sensitive animal 9 and up to 18 days in scrapings from containing Neethling strain (including and particularly well suited for the diagnosis dried lesions of air-dried hides held at room Lumpy Skin Disease Vaccine for Cattle® of capripox in less well equipped laboratories temperature. 10 The virus may be found in (Onderstepoort Biological Product, and in rural settings where resources are milk of infected animals; therefore, it should ); Lumpyvax®, Intervet, limited. 15 not be used as a supplement for susceptible Namibia; New live vaccine, HerbivacLS® Serological surveys for LSD virus are animals. 11 Deltamune/Ceva Santé Animale, South constrained by the lack of suitable diagnostic Africa); and tools. Unfortunately, there are no sufficiently • sheep pox vaccines produced in the sensitive and validated enzyme-linked region (including Sheep-pox vaccine immunosorbent assays (ELISAs) available

Table 2. Typical clinical signs for lumpy skin disease

Skin Mucosal lining Pregnant/lactating animals Other clinical signs Disseminated cutaneous Pox lesions may develop Reduction in milk yield by Fever, depression, anorexia, papules (2–5 cm) throughout throughout mucosa linings lactating cattle decreased weight gain and the full thickness of hide; of alimentary and respiratory emaciation necrotic centres (sitfasts), tracts, including nasal which may fall out, creating turbinates, trachea scars and holes in hide

Papules most easily seen in Pox lesions on lung with Possible abortions Excessive salivation, rhinitis and hairless areas of perineum, marked generalized interlobular conjunctivitis, which may be udder, inner ear and muzzle, edema, resulting in primary and mucopurulent eyelids secondary pneumonia Enlarged superficial lymph Legs may be edematous; nodes animal reluctant to move Secondary bacterial infections

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5. the likely impacts of LSD should for LSD virus. Although reliable, serum/virus pieces of tissue should be collected and movement occur. neutralization tests are labour-intensive and the medium should contain 10 percent Animal health authorities need this crucial time-consuming. This renders them unsuitable glycerol; the central part of the sample assessment in order to plan, implement and for large-scale testing. Moreover, since LSD can be used for virus isolation. manage subsequent activities to reduce the immunity is predominantly cell-mediated, Currently, there are two OIE Reference risk for spread and introduction of LSD in the serological assays may not reliably detect laboratories 16 for LSD confirmation: the region. antibody levels in vaccinated animals or Onderstepoort Veterinary Institute in South animals with mild clinical disease. The Western Africa and the Institute for Animal Health 2.2 Regional practices blot is highly sensitive and specific, but it is in the United Kingdom of Great Britain and expensive and difficult to perform. Northern Ireland. Communal grazing LSD is occurring in the Middle East and 1.9 Sample collection 1.10 Recent outbreaks Turkey in beef cattle raised in communal • Samples for virus isolation and antigen- in the region pastures and feedlots as well as in dairy detection ELISA should be taken during Between 6 August and 9 October 2013, cattle herds. Many countries in this region the first week of signs, before neutralizing four LSD outbreaks were reported in Turkey. are working towards instituting: i) vaccination antibodies have developed. Samples for They occurred along the eastern length of protocols; ii) quarantine measures; iii) national PCR can be collected after this time. the southern border with the Syrian Arab movement restrictions; iv) insect control; • In live animals, biopsy samples of skin Republic, Iraq and the Islamic Republic v) disinfection of infected premises; treatment nodules or lymph nodes can be used for of Iran. This outbreak followed the LSD of the affected animals with antipyretics and PCR, virus isolation and antigen detection. outbreaks in Israel, Lebanon, the West Bank antibiotics for secondary bacterial infections; Scabs, nodular fluid and skin scrapings and Jordan, which were reported between and in some cases v) culling of sick animals. may also be collected. July 2012 and September 2013 (Map A). Uncontrolled movements of • LSD virus can be isolated from blood livestock (particularly nomads) samples (collected into heparin or 2. Risk assessment ethylenediaminetetraacetic acid) during Uncontrolled livestock movements heighten the early, viraemic stage of disease; this is 2.1 Areas of risk the risk that LSD may move into additional unlikely to be successful after generalised areas of Turkey or LSD-free countries within lesions have been present for more than An urgent risk assessment for the region is the region. Examples include the documented, 4 days. required to help decision-makers understand: large, seasonal Kurdish transhumance • Samples of lesions, including tissues 1. where LSD outbreaks are occurring; movements in the southeast Anatolia region from surrounding areas, should be 2. what drivers may encourage LSD (see Map B). In addition, riverine agriculture submitted for histopathology. movement; and related activities at the deltas of the Tigris • Tissue and blood samples for virus 3. the risk of continued spread within and Euphrates rivers in Iraq have a potential isolation and antigen detection should currently affected countries; to be hot spots for vector transmission be kept chilled and shipped to the 4. the risk of LSD spread from (Map C). There is an immediate risk of LSD laboratory under proper cold chain infected countries to non-infected incursion into the Islamic Republic of Iran and conditions. If samples must be sent long countries; and the trans-caucasus countries. distances without refrigeration, large

Map A. Lumpy skin disease confirmed outbreaks. Observation dates from 01/07/2012 to 28/10/2013 (over estimated global cattle density).

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3. Risk management With the exception of options for at-risk vaccination, control measures Map C. Euphrates and Tigris rivers. countries are challenging to implement effectively. 3.1 Sanitary prophylaxis 3.2 Medical Free countries: prophylaxis • enforce import restrictions on livestock, At-risk, non infected countries carcasses, hides, skins and semen; should utilize: • enhance awareness of the disease; • homologous live • enhance capacity for symptomatic attenuated virus vaccine surveillance for LSD cases; (Neethling strain; • enhance laboratory capacity for LSD immunity lasts up to three testing; years); or • enhance rapid reporting regionally and • heterologous live internationally; and attenuated virus vaccine: • develop a prevention and response plan (Sheep or goat pox to include good emergency management vaccine, but may cause practices 17. local, sometimes severe, reactions). Infected countries: Follow manufacturer›s • implement strict quarantine measures instructions. Not advised in Source: http://en.wikipedia.org/wiki/File:Tigr-euph.png to avoid introduction of infected animals countries free from sheep and into safe herds; goat pox. • isolate animals and prohibit animal and differentials at the local cattle owner movement in the case of outbreaks; 3.3 Regional response plan level through extension veterinarians • slaughter all sick and infected animals components and other mechanisms to reach those dispose properly of dead animals A regional response plan is urgently needed. working daily with cattle and cattle (e.g. incineration); The plan should incorporate the below- owners and traders. • clean and disinfect premises and mentioned elements. • Provide incentives to notify suspicion of equipment; Information sharing within the disease. • control vectors in premises and on the country, regionally and Disease notification animals; and internationally • control vectors in ships and aircraft. • Immediately notify OIE when LSD is • Increase awareness about this disease suspected or diagnosed.

Map B. Large seasonal movements in southeast Anatolia.

Source: Thevenin Pastoralism: Research, Policy and Practice 2011 1:23 doi:10.1186/2041-7136-1-23

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2 Babiuk, S., Bowden, T. R., Boyle, D. B., Wallace, D. B. and Kitching, R. P. 2008. Capripoxviruses: An Emerging Worldwide Threat to Sheep, Goats and Cattle. Transboundary and Emerging Diseases. 55, 263–272 (available at http:// onlinelibrary.wiley.com/doi/10.1111/j.1865- 1682.2008.01043.x/pdf) 3 Chihota, C. M., L. F. Rennie, R. P. Kitching, and P. S. Mellor. 2001. Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae). Epidemiol. Infect. 126, 317–321. ©FAO/Eran Raizman ©FAO/Eran 4 Chihota, C. M., L. F. Rennie, R. P. Kitching, and P. S. Mellor. 2003. Attempted mechanical Strengthen local and regional insecticidal ground spraying, game transmission of lumpy skin disease virus by surveillance and laboratory capacity destruction or habitat clearance. biting insects. Med. Vet. Entomol. 17, 294–300. and networks 5 It is important to note that a limited number of • Identify/share standards for information 4. Conclusions studies have been conducted on LSD virus collection and exchange from field transmission by arthropod vectors. contacts: • The occurrence of LSD in Israel, Lebanon, 6 Irons, P. C., E. S. Tuppurainen, and E. H. »» Data collection Jordan, the West Bank and most recently Venter. 2005. Excretion of lumpy skin disease »» Data reporting in Turkey and likely Northern Iraq indicates virus in bull semen. Theriogenology. 63, »» Data analysis the potential for further spread of this 1290–1297. »» Response emerging disease to other countries in 7 Osuagwuh, U. I., V. Bagla, E. H. Venter, C. H. • Include surveillance support functions: the region and beyond where the cattle Annandale, and P. C. Irons. 2007. Absence of »» Training and supervision population is susceptible. lumpy skin disease virus in semen of vaccinated »» Laboratory strengthening • An urgent risk assessment for the bulls following vaccination and subsequent »» Communications region is required to help decision- experimental infection. Vaccine. Vol. 25, »» Resource management makers understand the situation and plan 2238–2243. »» Information collection – information response actions. 8 Lumpy Skin Disease. (available at http://www.oie. must be timely, complete, regular • Specific risk management options exist int/fileadmin/Home/eng/Animal_Health_in_ and of high quality, to be used for for at-risk countries, including sanitary the_World/docs/pdf/LUMPY_SKIN_DISEASE_ early detection and prediction of prophylaxis and medical prophylaxis as FINAL.pdf) epidemics, as well as to objectively well as the urgent need for regional 9 Onderstepoort J. Vet Res. 2005. Jun; 72(2): assess the effectiveness of coordination of prevention and control 153-64 interventions during the epidemics of the disease. Countries in the region 10 Weiss, K.E. 1968. Lumpy skin disease. Virol. and to provide efficient monitoring should develop and establish a regional Monogr., 3, 111-131. of established intervention response plan to facilitate coordination, 11 Davies, F.G. 1991. Lumpy skin disease, a programmes. information exchange and experience Capripox Virus Infection in Cattle in Africa. FAO, »» Use surveillance information to sharing. Rome, Italy. guide decisions with the goal to • FAO stands ready to provide 12 http://www.oie.int/fileadmin/Home/eng/Animal_ understand the extent of the spread assistance to member countries to Health_in_the_World/docs/pdf/LUMPY_SKIN_ of the disease and to implement an help reduce the risk of disease spread DISEASE_FINAL.pdf effective and appropriate response, and safeguard vulnerable, livestock- 13 http://www.discontools.eu/Diseases/Detail/86 using control measures designed to related livelihoods. Assistance should 14 The annual vaccination programme conducted stop the continued movement of the be focused on but not be limited to: in Ethiopia for local and Holstein Friesian disease. 18 i) disease early warning; ii) laboratory crossbreds reduced financial losses caused Use of appropriate vaccine capacity building; iii) risk management; by LSD by 17 and 31 percent per head, iv) surveillance; and v) control. respectively (Gari et al. 2001. Epidemiological • Identification of an effective vaccine to • At-risk countries would benefit aspects and financial impact of Lumpy Skin control LSD in a field setting is needed. from knowledge sharing by relevant Disease in Ethiopia. P.V.M. 102: 274-283). • Use of proper needle hygiene when countries in the region. FAO has the 15 http://jcm.asm.org/content/50/5/1613.full vaccinating herds, to avoid iatrogenic technical capacity, mandate and global 16 http://www.oie.int/?id=120? spread by people vaccinating the animals. network necessary to facilitate information 17 http://www.fao.org/docrep/014/ba0137e/ Supportive care exchange and promote collaboration. ba0137e00.pdf 18 http://www.who.int/csr/labepidemiology/ • Antibiotics to prevent secondary bacterial 5. References projects/surveillance/en infections 1 A recent study in Ethiopia found that the financial 19 http://www.ncbi.nlm.nih.gov/pubmed/19192613; Vector Control cost related to infected herds was estimated to http://sacemaquarterly.com/mathematical- be between USD 5–8 per head of local zebu modelling/modelling-the-control-of- • Insecticide-treated cattle (ITC) can be and between USD 42–73 per head of Holstein trypanosomiasis-using-trypanocides-or- effective, if re-treated between one and Friesian crossbred cattle (Gari et al. 2001. insecticide-treated-livestock.html; http://www. four weeks. 19 Epidemiological aspects and financial impact fao.org/docs/eims/upload/agrotech/1961/ • ITC is cheaper than vector control of Lumpy Skin Disease in Ethiopia. P.V.M. 102: CheapSafeTsetseControl.pdf methods, such as aerial spraying and 274-283). more environmentally friendly than 5 VOL 29 NOVEMBER 2013 | empres watch

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[email protected] or a fax to (+39) 06 57053023 Recommended citation FAO. 2013. Emergence of lumpy skin For more information visit us at http://www.fao.org/ag/empres.html disease in the Eastern Mediterranean Basin EMPRES-Animal Health can assist countries in the shipment of samples for TAD diagnostic testing at a countries. EMPRES WATCH, Vol. 29, FAO reference laboratory and reference centre. Please contact [email protected] for November 2013. Rome. information prior to sampling or shipment. Please note that sending samples out of a country requires an Back cover photo: ©FAO/Ivo Balderi export permit from the Chief Veterinarian’s Office of the country and an import permit from the receiving country.

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