LUMPY SKIN DISEASE IN BOVINE – A REVIEW
- MEERA P. SAKHARE1 AND DR. S. D. GAYAL2
- ASSISTANT PROFESSOR 2. M.V.SC. SCHOLAR
DEPARTMENT OF VETERINARY MEDICINE,
COLLEGE OF VETERINARY AND ANIMAL SCIENCES, MAFSU, PARBHANI (M.S.)
ABSTRACT
Lumpy skin disease is a vector borne, unnoticed viral disease caused by lumpy skin disease virus, a member of Capripoxvirus genus of Poxviridae family. LSD is an infectious and transboundary disease with economic importance affecting cattle. LSD causes eruptive skin lesions, occasionally fatal disease of cattle characterized by nodular growth on the skin and other parts of the body. The prominent clinical sign in LSD affected cattle were fever, anorexia and characteristic nodules on the skin mucous membrane of mouth, nostrils, udder, genital and rectum. In addition, drop in milk production, abortion, infertility and sometimes death were also recorded. The disease is commonly found in southern and eastern Africa, now it has spread to several countries in the middle east areas including India.
Keywords: Lumpy skin disease, bovine, transboundary disease, capripoxvirus
LUMPY SKIN DISEASE IN WORLD
Lumpy skin disease virus (LSDV) is a member of the genus Capripoxvirus, belongs to family poxviridae with typical poxvirus geomorphology and closely related to the viruses of sheep and goat pox. Lumpy skin disease is a significant transboundary bovine endemic disease in Africa and middle east countries and mediterrarian region (Gaud and Vijayakumar, 2020). The first outbreak of LSD was reported from Zambia in the year 1929 (Alexander et al., 1957) and the disease was termed as pseudo-urticaria (Weiss, 1968). In 1943, the condition was considered to be due to photosensitization (Quin and Dori, 1943) but the actual cause of LSDV was isolated in 1943 as capripoxvirus (Alexander et al., 1957) and was first time recognized as an infectious condition following an outbreak in Ngamiland, Northern Botswana (Von Backstrom, 1945). At the end of 1944, LSD was reported from South Africa where it spread rapidly throughout the country despite enforcement of control measures and the disease was invented as ‘Knopvelsiekte’ though also described as Pseudo-urticaria or Lumpy Disease or Ngamil and cattle disease (Thomas and Mari, 1945). The disease had become enzootic in 1947 in South Africa and also reported from Swaziland, Basutoland and Portuguese East Africa and subsequently from Madagascar, Tanganyika and Belgian Congo. LSD reported from Central and East Africa in 1956 and from Kenyain 1957 (MacOwan, 1959). Since then it has occurred widely in Africa and in Madagascar. In the year 1983, LSD was reported from Ethiopia and in 1988 from Egypt, Israel in 1989, Bahrain and Reunion in 1993, although those outbreaks were not confirmed by virus isolation (Coetzer et al., 2018). In the year 2006 and 2007 LSD was reported again in Egypt (Salib and Osman, 2011) and Israel and in the 2009 occurred in Oman (Brenner et al., 2009). During 2012-2013, LSD reappeared in northern Israel (Ben-Gera et al., 2015) and then spread rapidly in the Middle East, being reported in Lebanon, the Palestinian Autonomous Territories and Jordan and caused enormous economic losses (Abutarbush et al., 2015). Outbreaks of LSD was reported in Turkey (Timurkan et al., 2016) and in Kuwait, Saudi Arabia and Iraq (Al-Salihi and Hassan, 2015). In 2014, outbreaks of LSD were reported in Iran (Sameea et al., 2017) and the northern part of Cyprus as well as in Saudi Arabia and Bahrain. Then spread to northeast Caucasus, affecting Azerbaijan (Tasioudi et al., 2016). In 2015, it was recorded from Armenia and the Russian Federation. Lumpy skin disease was reported for the first time in the European union from Greece in 2015; it probably originated in Thrace (Turkey). In 2016, LSD occurred in Georgia and Kazakhstan. In 2016, LSD spread to Bulgaria, Serbia, Montenegro, Kosovo and Albania. In the same year it was reported again in Iran, Iraq and Azerbaijan (Coetzer et al., 2018).
LUMPY SKIN DISEASE IN INDIA
The first occurrence of LSD in India was reported to the OIE on 18th November, 2019 (OIE, 2019). Lumpy Skin Disease was introduced first time in the month of August 2019, in Odisha State of India as per (FAO, 2020). Out of 2539 animals presented, 182 were affected with LSD (Sudhakar et al., 2020) and in last year 2020, the disease was prevalent in state of Maharashtra and Madhya Pradesh. Lumpy skin disease may be alarm for pan India. During October 2019, LSD cases were also reported from Thrissur and Pallakad districts of Kerala and disease was first confirmed in Kerala (Goud and Vijaykumar, 2020). LSD has spread into several states of India including Kerala, Tamil Nadu, Andhra Pradesh, Telangana, Odisha, Jharkhand, West Bengal, Assam, Chhattisgarh, Maharashtra and Madhya Pradesh (Kumar et al., 2021). Lumpy skin disease reported in the native cattle and Asian water buffaloes around the tiger reserves of the central Indian highlands in Madhya Pradesh (Pandey et al., 2021).
ETIOLOGY
Lumpy skin disease (LSD) caused by lumpy skin disease virus (LSDV) which is associated to that of sheep pox virus. LSDV is a member of the genus Capripoxvirus within the subfamily Chordopoxvirinae, family Poxviridae. The prototype strain of LSD is known as the Neethling poxvirus (OIE, 2002 and Coetzer et al., 2018). All ages groups of cattle and both genders are susceptible to LSDV infection (Weiss, 1968) although on occasion cows have been only mildly affected while their calves developed more typical and severe lesions 24 to 48 hours earlier than their dams (Le Roux, 1945). More severe disease has been reported in exotic breeds of cattle i.e. Holstein Friesian, especially those with thin skins such as Friesians and in other high producing European dairy breeds. Cows in peak lactation seems to be more severely affected (Coetzer et al., 2018). It has been observed that Holstein Friesian cattle or crossbred cattle are more susceptible to LSD as compared to zebu cattle (OIE, 2002).
TRANSMISSION
The exact mode of transmission of LSDV is unidentified, however it has been suggested that the illness is spread by arthropod vectors (Gupta et al., 2020). Three African hard tick species have been confirmed to physiologically transmit the virus in lab tests. Contact infection is considered another route of infection since the illness has been experimentally transmitted via contaminated saliva. In Kenya, African buffalo are thought to be act as maintenance hosts.
Vectors: Aedes aegypti female mosquitoes and sheep head flies are capable for mechanical transmission of LSDV from infected to susceptible cattle (Chihota et al., 2001, Kitching and Mellor, 1986 and MacLachlan and Dubovi, 2011). Mosquitoes fed upon lesions of cattle infected with LSDV were able to transmit virus to susceptible cattle over a period of 2–6 days post-infective feeding (Wallace et al., 2006). An abundance of the Stomoxys flies was associated with outbreaks of LSD. The transmission studies revealed that Rhipicephalus (Boophilus) appendiculatus male tick transmit LSDV mechanically. Similarly, decoloratus females were shown to transmit the virus via their eggs to larvae, which in turn, were able to infect the cattle (Coetzer et al., 2018). In saliva and other organs of ticks, including haemocytes, salivary glands, and midgut, the lumpy skin disease virus and viral antigen were discovered (Lubinga et al., 2013).
Semen: The LSDV has been isolated from the semen of inapparent affected bulls (Weiss, 1968, Sudhakar et al., 2020 and Tuppurainen et al., 2017). Transmission of LSDV via artificial insemination has also been revealed experimentally (Annandale et al., 2014 and Irons et al., 2005).
Fomites: LSDV transmission can occur when common drinking and feeding troughs were used, thus confirming the suspicion that infected saliva may contribute to the spread of the disease (Coetzer et al., 2018).
Direct contact: The disease is transmissible to suckling calves through contaminated milk and infected cows have been reported to give birth to calves with skin lesions (Coetzer et al., 2018). The transmission mostly occurs by indirect contact, probably by flying, blood-sucking insects and has important implications for control of LSD (Magori-Cohen et al., 2012).
Iatrogenic transmission: The transmission via contaminated needles during vaccination or other injections may also occur (Coetzer et al., 2018).
Season: Majority of LSD outbreaks have occurred during the summer, when arthropods are most active, this might imply that several vector species, predominantly blood-feeding insects, are involved in viral dissemination (Kahana-Sutin et al., 2017; Sprygin et al., 2018 and Namazi and Tafti et al., 2021). Seasonal variation in the force of LSD infection associated with temperature, possibly through its influence on the relative abundance of the stable fly, stomoxys calcitrans (Gubbins et al., 2020).
CLINICAL SIGNS
Lumpy skin disease (LSD) may observed in three stages; acute, subacute, and chronic (Gari et al., 2010). In experimental conditions, the disease incubation period ranges from 4 to 14 days, however in natural infection, the incubation period is 2 to 5 weeks (Carn and Kitching, 1995; Tuppuraine et al., 2005; Ahmed et al., 2020). Skin lesions were common on the head, neck, udder, genitalia, perineum and legs. While, superficial lymph nodes were enlarged and oedematous (Prozesky and Barnard 1982; Davies, 1991).
Skin nodules all over the body, fever (may exceed 41°C) that lasts 6 to 72 hours, lacrimal discharge, nasal discharge, anorexia, decreased milk yield, emaciation, depression, and reluctance to move (Al-Salihi, 2014). Observed skin nodules on the muzzle, nares, back, limbs, scrotum, udder, perineum, eyelids, ears, nasal mucosa, oral mucosa, and tail (Salib and Osman, 2011). Skin nodules may disappear, but sometimes these may persist as hard lumps or become moist, necrotic and ulcerated. The ulcerated lesions may create a hole in the skin (Abutarbushet al., 2013). These ulcerated lesions may be contaminated by secondary bacterial complication and infestation of fly worms (Amenu et al., 2018).
The subscapular and prefemoral lymph nodes had become enlarged to 3-5 times of their normal size and easily palpable (Tuppurainen et al., 2017). Edematous and inflammatory swellings of the face, brisket and one or more limbs, may be seen leading to difficulties in movement. In some cases, unilateral or bilateral keratitis may be observed in infected animals (Jameel, 2016). Pneumonia is a common sequel in animals affected by LSD with lesions in the mouth and respiratory tract (Al-Salihi, 2014). Females infected with the LSD can causes anestrus for months or become sterile due to poor body condition and other stress factors (Al-Salihi, 2014). In some cases, the affected pregnant animals may abort. In infected bulls, there may be orchitis leading to infertility to sterility (Sarma, 2009). Clinical findings like fever, skin nodules on the neck, back, perineum, tail, hind limbs and genital organs, enlarged superficial lymph nodes and, in some cases, legs and brisket edema along with lameness were also reported by (Hunter and Wallace 2001, Brenner et al., 2006, Al-Salihi and Hassan, 2015, Abutarbush et al. 2015, Kumar et al., 2020, Sudhakar et al., 2020, Pandey et al., 2021 and Sethi et al., 2021).
Large (3–8 cm) skin nodules are characteristic, sometimes accompanied by fever, occulo-nasal discharge and swollen lymph nodes. Nodules have been reported on the neck, nares, muzzle, back, legs, perineum, scrotum, eyelids, ears, nasal mucosa, and tail (Al-Salihi and Hassan, 2015). A characteristic inverted conical zone of necrosis has been described (Abutarbush et al., 2015). Oedema of the face, brisket and limbs was sometimes seen in LSD affected animals (Hunter and Wallace, 2001; Salib and Osman 2011; Tageldin et al., 2014). Sloughing lesions produced “sitfast” hole shape, the usual lesion that subsequently triggers screwworm fly invasion and invasion of bacteria which can additional aggravate to septicaemia (Constable et al., 2017).
DIAGNOSIS
Diagnosis of LSD is often based on characteristic clinical signs and clinical diagnosis. In naturally infected animals clinical manifestations observed were lachrymation, nasal discharge, enlarged lymph nodes, high fever, drop in milk yield, generalized skin nodules, necrotic pox lesions around muzzle, skin lesions on the legs and secondary bacterial infections, deep scab, formations (sit-fast) and mastitis ( Rozstalny et al., 2017). Effective control or eradication of LSD in endemic and non-endemic areas requires rapid and accurate diagnostic methods to confirm a presumptive diagnosis (Tuppurainen et al., 2005). However, mild and subclinical forms require rapid and reliable laboratory testing to confirm diagnosis (Soliman and Abdelrahman, 2008). Most commonly used methods of diagnosing LSD are detecting LSDV DNA which is most rapidly done by using the polymerase chain reaction (PCR) test (Gelaye et al., 2017). A variety of molecular tests using Capripoxvirus-specific primers are considered sensitive and specific for LSDV identification (Goff et al., 2009 and Gelaye et al., 2013). Electron microscopy can be used to identify the classic poxvirus virion but cannot differentiate to genus or species level (OIE, 2010) and virus isolation using cell culture followed by PCR is important to confirm the virus identity (Bowden et al., 2008).
Virus isolation on primary or secondary bovine dermis cells or lamb testis cells is considered to be the most sensitive. All CaPVs share a common major antigen for neutralizing antibodies, therefore; it is not possible to distinguish strains of CaPVs using serology based diagnostic techniques (OIE, 2010). Virus neutralization tests and electron microscopy examination are widely used as gold standard methods for the detection of CaPV infection (Bowden et al., 2008). Serological assay methods such as indirect enzyme linked immuno-sorbent assay (iELISA), western blotting, agar gel immuno-diffusion test and the indirect fluorescent antibody test are also used to diagnose LSD. However, Serological assessment of antibodies to a CaPVs may sometimes be difficult due to the crossreactivity encountered with other poxviruses as well as to the low antibody titers elicited in some animals following mild infection or vaccination. Therefore, PCR was the test of choice for rapid detection and identification of the LSD outbreak causative agents (OIE, 2010).
DIFFERENTIAL DIAGNOSIS
The milder forms of LSD could be confused with other diseases producing skin lesions such as pseudo-lumpy skin disease (bovine herpesvirus-2 infection), insect bites, demodecosis and dermatophilosis. Moreover, disease causing mucosal lesions, such as rinderpest, bovine viral diarrhea/mucosal disease, and bovine malignant catarrhal fever, also creates field diagnosis complex (OIE, 2010).
Pseudo-lumpy skin disease: A much milder disease caused by a Herpesvirus.
Bovine Herpes mammillitis: Lesions were generally confined to the teats andudder.
Urticaria: skin condition characterized by development of topical dermal edema becoming apparent as cutaneous wheals, commonly seen in horses.
Dermatophilosis / streptothricosis: Nonpruritic crusting dermatitis, initially with paintbrush tufts of hair. In tropical areas, extensive skin lesions seen in cattle.
Demodicosis: The pustular form nodules with pus filled lesions.
Cow pox: Pustular eruptions on the forelimb or face accompanied by slight fever and lymphadenitis.
Vesicular stomatitis: Vesicles and erosions of the mucosa of gum, tongue, muzzle and skin of the coronary band commonly noticed.
Bovine ephemeral fever: Inflammatory disease with enlargement of lymph node, fever, nasal discharge, shifting lameness with short clinical course.
Photosensitization: dermal sign started with erythema, itching, oedema and irritation, necrosis, gangrene and exfoliation or sloughing of the superficial skin layer. Demarcation with affected and healthy skin.
Besnoitiosis (elephant skin disease): Exudative dermatitis characterized by thickening, folding of skin, hair loss, cracks, scabs, edema and enlargement of superficial lymph nodes.
(Constable et al.,2017 and Scott, 2016).
SOCIO-ECONOMIC IMPACT
The LSDV usually causes 10-20% morbidity and 1-5% mortality among the livestock (OIE, 2017), but other studies have reported 100% morbidity (Gupta et al., 2020). Total losses of 51,590 USD from death of 108 cattle had been calculated in central Ethiopia (Ayelet et al., 2014). Usually, mortality rate is 1-5% (OIE, 2002), however, it is variable depending on the strain of virus and its virulence and susceptibility of host; 50% in young animals, 5% in adults (FAO, 1994). Epidemiological aspects and economic impact of LSD studied by (Amenu et al., 2018).LSD is economically important because of its prolonged debilitating effects in severely afflicted animals including reduced weight-gain, temporary or permanent cessation of milk production, sometimes accompanied by mastitis, temporary or permanent infertility or even sterility in bulls as a consequence of orchitis, as well as permanent skin damage. Abortion may follow infection in approximately 10% of pregnant cows (Coetzer et al., 2018).LSD causes high economic losses due to chronic debility in affected cattle, reduced milk production, poor growth, infertility, abortion and sometimes death. The risk factor of LSD infection between breeds showed that HF/crossbreds had higher odds of becoming affected than the local zebu breed. Whereas, occurrence of LSD infection was more in male local zebu cattle than in females (Gari et al., 2011).
CONCLUSION
Lumpy skin disease is an emerging transboundary viral disease of cattle with economic importance. Prominent clinical signs in LSD affected cattle was fever, generalised skin nodules, oculo-nasal discharge, brisket oedema, enlarged superficial lymph nodes and anorexia.The most reliable confirmative molecular diagnosis of LSDV by PCR and iELISA. The transmission of LSDV can be effectively done by control of insect vectors.
REFERENCES
http://ijah.in/upload/snippet/280_66.pdf
Abutarbush, S.M., Ababneh, M.M., Al Zoubi, I.G., Al Sheyab, O.M., Al Zoubi, M.G., Alekish, M.O. and Al Gharabat, R.J. (2015) Lumpy Skin Disease in J ordan: Disease Emergence, Clinical Signs, Complications and Preliminary‐associated Economic Losses. Transboundary and emerging diseases.62 (5): 549-554.
Alexander, R.A., Plowright, W. and Haig, D.A. (1957) Cytopathogenic agents associated with lumpy skin disease of cattle.Bulletin of epizootic diseases of Africa.5 :489-492.
Al Salihi, K.A. and Hassan, I.Q. (2015) Lumpy skin disease in Iraq: study of the disease emergence. Transboundary and emerging diseases.62 (5) :457-462.
Annandale, C.H., Holm, D.E., Ebersohn, K. and Venter, E.H. (2014) Seminal transmission of lumpy skin disease virus in heifers. Transboundary and emerging diseases, 61(5): 443-448.
Ben-Gera, J., Klement, E., Khinich, E., Stram, Y. and Shpigel, N.Y. (2015) Comparison of the efficacy of Neethling lumpy skin disease virus and x10RM65 sheep-pox live attenuated vaccines for the prevention of lumpy skin disease–The results of a randomized controlled field study. Vaccine, 33(38) : 4837-4842.
Brenner, J., Bellaiche, M., Gross, E., Elad, D., Oved, Z., Haimovitz, M., Wasserman, A., Friedgut, O., Stram, Y., Bumbarov, V. and Yadin, H. (2009) Appearance of skin lesions in cattle populations vaccinated against lumpy skin disease: statutory challenge. Vaccine, 27(10): 1500-1503.
Chihota, C.M., Rennie, L.F., Kitching, R.P. and Mellor, P.S. (2001) Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae). Epidemiology & Infection, 126(2) :317-321.
Coetzer, J.A.W, Tuppurainen, E., Babiuk, S. and Wallace, D. (2018) Lumpy Skin Disease. In book: Infectious Diseases of Livestock, Part II Publisher: Anipedia.
Coetzer, J.A.W. and Tuppurainen, E. (2004) Lumpy skin disease. Infectious diseases of livestock, 2, Pp.1268-1276.
Davies, F.G. (1991) Lumpy skin disease of cattle: a growing problem in Africa and the Near East. World Animal Review, 68(3) :37-42.
Diesel, A.M. (1949) The epizootology of “lumpy skin disease” in South Africa. Proc. 14th International Veterinary Congress, London 2, 492–500.
El-Nahas, E.M., El-Habbaa, A., El-Bagoury, G. and Radwan, M.E. (2011) Isolation and identification of lumpy skin disease virus from naturally infected buffaloes at Kaluobia, Egypt. Global Veterinaria, 7(3) :234-237.
FAO (1994) Manual on meat inspection for developing countries. Food and Agriculture Organization of the United Nations Rome.
Gupta, T., Patial, V., Bali, D., Angaria, S., Sharma, M. and Chahota, R. (2020) A review: Lumpy skin disease and its emergence in India. Veterinary Research Communications, pp.1-8.
Haig, D.A. (1957) Lumpy skin disease. Bull. Epizoot. Dis. Afr, 5(9): 421–430.
Irons, P.C., Tuppurainen, E.S.M. and Venter, E.H. (2005) Excretion of lumpy skin disease virus in bull semen. Theriogenology, 63(5) :1290-1297.
Kitching, R.P. and Mellor, P.S. (1986) Insect transmission of capripoxvirus. Research in veterinary science, 40(2), pp.255-258.
Le Roux, P.L. (1945) Notes on the probable cause, prevention and treatments of pseudo-urticaria and associated septic conditions in cattle. Northern Rhodesia Department of Animal Health, Newsletter, pp.1-4.
MacOwan, K.D.S. (1959) Observations on the epizootiology of lumpy skin disease during the first year of its occurrence in Kenya. Bull. Epizootic Dis. of Africa, 7, pp.7-20.
OIE, (2002) LUMPY SKIN DISEASE – Aetiology Epidemiology Diagnosis Prevention and Control References. P. 5.
Punniamurthy N., Ethnoveterinary formulation for Lumpy Skin Disease For oral administrations. National dairy Development Board.
Quin, J.L. and Dori J.L. (1943) A skin condition in cattle probably associated with photosensitisation. Journal of the South African Veterinary Association, 14(1) : 10-11.
Salib, F.A. and Osman, A.H. (2011) Incidence of lumpy skin disease among Egyptian cattle in Giza Governorate, Egypt. Veterinary World, 4(4).
Sameea Yousefi, P., Mardani, K., Dalir Naghadeh, B. and Jalilzadeh Amin, G. (2017) Epidemiological study of lumpy skin disease outbreaks in North western Iran. Transboundary and emerging diseases, 64(6) : 1782-1789.
Sudhakar, S.B., Mishra, N., Kalaiyarasu, S., Jhade, S.K., Hemadri, D., Sood, R., Bal, G.C., Nayak, M.K., Pradhan, S.K. and Singh, V.P. (2020) Lumpy skin disease (LSD) outbreaks in cattle in Odisha state, India in August 2019: Epidemiological features and molecular studies. Transboundary and Emerging Diseases.
Tasioudi, K.E., Antoniou, S.E., Iliadou, P., Sachpatzidis, A., Plevraki, E., Agianniotaki, E.I., Fouki, C., Mangana Vougiouka, O., Chondrokouki, E. and Dile, C. (2016) Emergence of lumpy skin disease in Greece, 2015. Transboundary and Emerging Diseases, 63(3) : 260-265.
Thomas, A.D. and Mari C.V.E. (1945) Knopvelsiekte. Journal of the South African Veterinary Association, 16(1) : 36-43.
Timurkan, M.O., Ozkaraca, M., Aydın, H. and Sağlam, Y.S. (2016) The detection and molecular characterization of lumpy skin disease virus, northeast Turkey. International Journal of Veterinary Science, 5(1) : 44-47.
Von Backstrom, U. (1945) Ngamiland cattle disease: preliminary report on a new disease, the etiological agent being probably of an infectious nature. Journal of the South African Veterinary Association, 16(1) : 29-35.
Wallace, D.B., Ellis, C.E., Espach, A., Smith, S.J., Greyling, R.R. and Viljoen, G.J., (2006) Protective immune responses induced by different recombinant vaccine regimes to Rift Valley fever. Vaccine, 24 (49-50) : 7181-7189.
Weiss, K.E. (1968) Lumpy skin disease virus. In Cytomegaloviruses. Rinderpest Virus. Lumpy Skin Disease Virus (pp. 111-131). Springer, Berlin, Heidelberg.
