Br. vet . J (1991) . 147, 4 8 9
SPECIAL REVIEW SERIES
LUMPY SKIN DISEASE, AN AFRICAN CAPRIPOX VIRUS DISEASE OF CATTLE
F . G . DAVIES* Veterinary Research Laboratory, PO Kabete, Kenya
SUMMARY Lumpy skin disease is an infectious viral disease of cattle, which often occurs in epizootic form . The disease is characterized by the eruption of nodules in the skin, which may cover the whole of the animal's body . Systemic effects include pyrexia, anorexia, dysgalactia and pneumonia ; lesions are often found in the mouth and upper respiratory tract. The severity of the disease varies considerably between breeds and strains of cattle . Many cattle suffer severe emaciation and loss of production for several months . The skin lesions cause permanent damage to the hides . The mode of transmission of the disease has not been clearly established . Contact infections do not readily occur and the evidence from the epizootiology strongly suggests that insect vectors are involved . The disease has been confined to sub-Saharan Africa, until it recently appeared in epizootic form in Egypt and in Israel . Transmission occurs in a wide variety of biotypes, from semi-desert to temperate grasslands and irrigated land . It has the potential to extend its range further .
INTRODUCTION Lumpy skin disease (LSD) was first identified in Northern Rhodesia (Zambia) in 1929 (MacDonald, 1931) where it was first thought to be an allergic reaction to insect bites . The syndrome recurred irregularly there until 1943, when it spread to Botswana (Bechuanaland) (von Backstrom, 1945) and in 1945 to Zimbabwe (Southern Rhodesia) (Huston, 1945), and to South Africa (Thomas & Mare, 1945) . The transmissible nature of the disease became apparent to South African workers (Thomas & Mare, 1945 ; von Backstrom, 1945) during an epizootic which * Present address : G2 The Court, St . Mary's Place, Shrewsbury SYl 1 DY, U .K.
490
BRITISH VETERINARY JOURNAL, 147,6
affected most of the country . Some 8 million cattle were involved in this outbreak with enormous economic losses (Diesel, 1949) . In 1957, LSD was identified in East Africa, where it has recurred at intervals ever since (Burdin & Prydie, 1959) . Epizootics were reported from the Nile basin in the Sudan in the 1970s and during the period 1970-1985 LSD occurred in most Central and West African countries (Annual Reports FAO/OIE) . The disease is now enzootic throughout sub-Saharan Africa (including Madagascar) and recently appeared in Egypt in 1988 (Ali Moussa, personal communication, 1989) and in Israel in 1989 (Shimshony, 1989) . LSD extended from a focus in Ismailyia in Egypt and largely in the summer months of 1989, infected cattle in 22 of the 26 Governates of Egypt . Cases occurred from Aswan to the delta and also in the desert oasis well away from the Nile itself . The disease is now enzootic in Egypt . An extension has occurred eastwards into Israel, probably by the movement of insect vectors . Further spread westward may occur despite all the control strategies . The significance of an overlap in the distribution of LSD with Cochliomyia hominivorax in North Africa is great, for the multiple necrotic foci of the LSD lesions furnish ideal oviposition sites for the fly . Despite the success of the control measures, this remains a possibility . LSD has occurred in all the diverse ecological zones in Africa, from the high altitude temperate grasslands, the wet and dry bushed and wooded savannah to the very dry semi-desert . It has caused epizootics in irrigated areas of Africa and Egypt . Clearly, the potential exists for spread beyond its historical range, into North Africa, the Middle East and northern Mediterranean countries .
AETIOLOGY The initial observations suggested that the disease was an allergic response to insect bites (Morris, 1931) which was supported by the prevalence of the condition after the rains, when biting insect populations were at their highest . Experimental studies in South Africa (Thomas & Mare, 1945 ; von Backstrom 1945) showed that a transmissible agent was involved . The early attempts to identify this in tissue cultures were hampered by the simultaneous isolation of two different herpesviruses from LSD or similar lesions (Alexander et al., 1957) . A bovine herpesvirus 2 (Allerton or pseudo-lumpy skin disease virus) was isolated, which produces skin lesions which are very similar to LSD in the early stages (Alexander et al., 1957 ; Haig, 1957 ; Weiss, 1968 ; Davies et al., 1971) . A bovine herpesvirus 3 was also isolated from LSD tissue biopsy material but this caused no pathological changes in bovine skin when inoculated from infected tissue cultures (Alexander et al., 1957) . The third group of viruses isolated was of the pox type . They reproduced the disease when tissue culture harvests were reinoculated into susceptible cattle (Alexander et al., 1957) . Their morphology and physical characteristics were similar to those of the orthopoxviruses . Serological and immunological tests showed that they were capripoxviruses, very closely related to sheep and goat pox viruses (SGPV) (Capstick, 1961 ; Davies & Atema, 1981) . Most strains of these protect cattle against LSD when inoculated into cattle and LSD virus protects sheep and
LUMPY SKIN DISEASE
49 1
goats against capripox disease . Serological studies by immunofluorescence and virus-serum neutralization have not shown any differences between strains of LSD and of SGPV (Davies & Atema, 1981) . The strains of LSD thus far examined have all proved to be serologically identical (Davies, 1982) . Restriction enzyme studies suggest that LSD strains are identical and that their genome appears to be the same as that of the Kenya SGPV (KSGPV) (Black et al., 1986) . There are differences, however, between LSD and many of the SGPV from the Middle East and elsewhere (Gershon & Black, 1988 ; Kitching et al., 1989) .
CLINICAL SIGNS LSD is an acute infectious disease of cattle of all ages, well described by MacDonald (1931), von Backstrom (1945) and Ayre-Smith (1960) . There has recently been a clinical report of the disease in the Asian water buffalo (Bubalis bubalis), where five cases were observed in a group of 300 (Ali et al., 1990) . The incubation period after experimental inoculation is 4-12 days, usually about 7 days . The introduction of infected cattle is followed by disease in 2-5 weeks . There is a pyrexia of 40 .0-41 .5°C which may last 1-10 days . This is accompanied by lachrymation, increased nasal and pharyngeal secretions, anorexia, dysgalactia, some depression and a disinclination to move . Within 1-2 days, there is a cutaneous eruption of nodules, which may cover the whole of the body, while in other animals only a few may develop . The predilection sites are the head and neck, perineum, genitalia and udder, and the limbs (Figs 1-3) . The nodules are 5-50 mm or more in diameter, appearing as circumscribed areas of erect hair, firm and slightly raised from the surrounding normal skin . There is hyperaemia and drops of serum appear on the affected skin surface . The lesions are of a full skin thickness involving the epidermis, dermis and subcutis, which may be oedematous . The regional lymph nodes are enlarged and oedematous . Lesions develop on the muzzle, in the nares and oropharynx . They show a ringlike margin, where there has been separation from the surrounding healthy epithelium . Lesions may develop in the larynx and trachea, throughout the alimentary tract, and especially in the abomasum . They become necrotic and ulcerate . Mucopurulent nasal discharges, persistent dribbling of infected saliva, coughing and stertorious and often distressed respiration result . Conjunctivitis and keratitis commonly occur (Fig . 4) . Inflammatory and oedematous swellings of the limbs, brisket and genitalia may develop; the limbs can be three to four times their normal size (Fig . 5) . The lesions become necrotic and while some remain in situ, where they are recognizable for at least a year, others slough away to leave a full skin thickness hole, which usually becomes infected by suppurative bacteria . Larger areas of skin over a hard oedematous limb may become necrotic and slough away leaving a huge raw area ripe for bacterial infection and myasis . Herein lies the danger for infestation by Cochliomyia hominivorax. Lesions on the udder and teats may cause a mastitis and oedema with secondary infections and can result in sloughing of mammary tissue . Other nodular lesions develop in the subcutis, and may also be distributed throughout the connective tissue and muscles of the limbs and body .
492
LUMPY
Fig.
5.
SKIN
DISEASE
A limb swollen as a result of ISD infection.
Pneumonia is a common and often fatal complication of LSD. I,esions may be found throughout the upper respiratory tract and focal or larger areas of grey consolidation may develop in the lungs together with larger areas of bronchopneumania. Inhalation is a sequel of the necrotic lesions in the respiratory tract and it may prove f’ntal even months after the initial infection when a necrotic slough 1947). The pneumonias rarel, OCCL~ from an old tracheal lesion (de Boom, rrspond to antibiotic therapy. Xhortion frequently follows the acute infection in females, and infertility has been a problem in the months succeeding an outbreak. Bulls may have painful lesions of their genitalia, which can prevent them serving, and may remain infertile for 3-6 months after the disease. Females mav be anoestrous for se\~ral months. These effects are thought to he a consequence of the serious loss in COIIdition associated with LSD. Fetuses may be aborted, or the skin of calvrs t,orlI after an epi/ootic may be covered with lesions of ISD (Davies, unpublished data). Such intrauterine infections have also been described with swinepox ( BOI-st r/ (I/., 1990). Extensive skin lesions which produce a hidehourld condition, limb oedema and mouth and respirator-v lesions mav cause a prolonged anorexia and disinclination to I~OVC~. Rapid dete&ration in body condition follows and, LII~~CIrange COIIditions, the illability to move to water results in a higher mortality from dehvdration and predators. Some cattle become so emaciated that euthanasia is indicated.
SPECIAL REVIEW SERIES
LUMPY SKIN DISEASE, AN AFRICAN CAPRIPOX VIRUS DISEASE OF CATTLE
F . G . DAVIES* Veterinary Research Laboratory, PO Kabete, Kenya
SUMMARY Lumpy skin disease is an infectious viral disease of cattle, which often occurs in epizootic form . The disease is characterized by the eruption of nodules in the skin, which may cover the whole of the animal's body . Systemic effects include pyrexia, anorexia, dysgalactia and pneumonia ; lesions are often found in the mouth and upper respiratory tract. The severity of the disease varies considerably between breeds and strains of cattle . Many cattle suffer severe emaciation and loss of production for several months . The skin lesions cause permanent damage to the hides . The mode of transmission of the disease has not been clearly established . Contact infections do not readily occur and the evidence from the epizootiology strongly suggests that insect vectors are involved . The disease has been confined to sub-Saharan Africa, until it recently appeared in epizootic form in Egypt and in Israel . Transmission occurs in a wide variety of biotypes, from semi-desert to temperate grasslands and irrigated land . It has the potential to extend its range further .
INTRODUCTION Lumpy skin disease (LSD) was first identified in Northern Rhodesia (Zambia) in 1929 (MacDonald, 1931) where it was first thought to be an allergic reaction to insect bites . The syndrome recurred irregularly there until 1943, when it spread to Botswana (Bechuanaland) (von Backstrom, 1945) and in 1945 to Zimbabwe (Southern Rhodesia) (Huston, 1945), and to South Africa (Thomas & Mare, 1945) . The transmissible nature of the disease became apparent to South African workers (Thomas & Mare, 1945 ; von Backstrom, 1945) during an epizootic which * Present address : G2 The Court, St . Mary's Place, Shrewsbury SYl 1 DY, U .K.
490
BRITISH VETERINARY JOURNAL, 147,6
affected most of the country . Some 8 million cattle were involved in this outbreak with enormous economic losses (Diesel, 1949) . In 1957, LSD was identified in East Africa, where it has recurred at intervals ever since (Burdin & Prydie, 1959) . Epizootics were reported from the Nile basin in the Sudan in the 1970s and during the period 1970-1985 LSD occurred in most Central and West African countries (Annual Reports FAO/OIE) . The disease is now enzootic throughout sub-Saharan Africa (including Madagascar) and recently appeared in Egypt in 1988 (Ali Moussa, personal communication, 1989) and in Israel in 1989 (Shimshony, 1989) . LSD extended from a focus in Ismailyia in Egypt and largely in the summer months of 1989, infected cattle in 22 of the 26 Governates of Egypt . Cases occurred from Aswan to the delta and also in the desert oasis well away from the Nile itself . The disease is now enzootic in Egypt . An extension has occurred eastwards into Israel, probably by the movement of insect vectors . Further spread westward may occur despite all the control strategies . The significance of an overlap in the distribution of LSD with Cochliomyia hominivorax in North Africa is great, for the multiple necrotic foci of the LSD lesions furnish ideal oviposition sites for the fly . Despite the success of the control measures, this remains a possibility . LSD has occurred in all the diverse ecological zones in Africa, from the high altitude temperate grasslands, the wet and dry bushed and wooded savannah to the very dry semi-desert . It has caused epizootics in irrigated areas of Africa and Egypt . Clearly, the potential exists for spread beyond its historical range, into North Africa, the Middle East and northern Mediterranean countries .
AETIOLOGY The initial observations suggested that the disease was an allergic response to insect bites (Morris, 1931) which was supported by the prevalence of the condition after the rains, when biting insect populations were at their highest . Experimental studies in South Africa (Thomas & Mare, 1945 ; von Backstrom 1945) showed that a transmissible agent was involved . The early attempts to identify this in tissue cultures were hampered by the simultaneous isolation of two different herpesviruses from LSD or similar lesions (Alexander et al., 1957) . A bovine herpesvirus 2 (Allerton or pseudo-lumpy skin disease virus) was isolated, which produces skin lesions which are very similar to LSD in the early stages (Alexander et al., 1957 ; Haig, 1957 ; Weiss, 1968 ; Davies et al., 1971) . A bovine herpesvirus 3 was also isolated from LSD tissue biopsy material but this caused no pathological changes in bovine skin when inoculated from infected tissue cultures (Alexander et al., 1957) . The third group of viruses isolated was of the pox type . They reproduced the disease when tissue culture harvests were reinoculated into susceptible cattle (Alexander et al., 1957) . Their morphology and physical characteristics were similar to those of the orthopoxviruses . Serological and immunological tests showed that they were capripoxviruses, very closely related to sheep and goat pox viruses (SGPV) (Capstick, 1961 ; Davies & Atema, 1981) . Most strains of these protect cattle against LSD when inoculated into cattle and LSD virus protects sheep and
LUMPY SKIN DISEASE
49 1
goats against capripox disease . Serological studies by immunofluorescence and virus-serum neutralization have not shown any differences between strains of LSD and of SGPV (Davies & Atema, 1981) . The strains of LSD thus far examined have all proved to be serologically identical (Davies, 1982) . Restriction enzyme studies suggest that LSD strains are identical and that their genome appears to be the same as that of the Kenya SGPV (KSGPV) (Black et al., 1986) . There are differences, however, between LSD and many of the SGPV from the Middle East and elsewhere (Gershon & Black, 1988 ; Kitching et al., 1989) .
CLINICAL SIGNS LSD is an acute infectious disease of cattle of all ages, well described by MacDonald (1931), von Backstrom (1945) and Ayre-Smith (1960) . There has recently been a clinical report of the disease in the Asian water buffalo (Bubalis bubalis), where five cases were observed in a group of 300 (Ali et al., 1990) . The incubation period after experimental inoculation is 4-12 days, usually about 7 days . The introduction of infected cattle is followed by disease in 2-5 weeks . There is a pyrexia of 40 .0-41 .5°C which may last 1-10 days . This is accompanied by lachrymation, increased nasal and pharyngeal secretions, anorexia, dysgalactia, some depression and a disinclination to move . Within 1-2 days, there is a cutaneous eruption of nodules, which may cover the whole of the body, while in other animals only a few may develop . The predilection sites are the head and neck, perineum, genitalia and udder, and the limbs (Figs 1-3) . The nodules are 5-50 mm or more in diameter, appearing as circumscribed areas of erect hair, firm and slightly raised from the surrounding normal skin . There is hyperaemia and drops of serum appear on the affected skin surface . The lesions are of a full skin thickness involving the epidermis, dermis and subcutis, which may be oedematous . The regional lymph nodes are enlarged and oedematous . Lesions develop on the muzzle, in the nares and oropharynx . They show a ringlike margin, where there has been separation from the surrounding healthy epithelium . Lesions may develop in the larynx and trachea, throughout the alimentary tract, and especially in the abomasum . They become necrotic and ulcerate . Mucopurulent nasal discharges, persistent dribbling of infected saliva, coughing and stertorious and often distressed respiration result . Conjunctivitis and keratitis commonly occur (Fig . 4) . Inflammatory and oedematous swellings of the limbs, brisket and genitalia may develop; the limbs can be three to four times their normal size (Fig . 5) . The lesions become necrotic and while some remain in situ, where they are recognizable for at least a year, others slough away to leave a full skin thickness hole, which usually becomes infected by suppurative bacteria . Larger areas of skin over a hard oedematous limb may become necrotic and slough away leaving a huge raw area ripe for bacterial infection and myasis . Herein lies the danger for infestation by Cochliomyia hominivorax. Lesions on the udder and teats may cause a mastitis and oedema with secondary infections and can result in sloughing of mammary tissue . Other nodular lesions develop in the subcutis, and may also be distributed throughout the connective tissue and muscles of the limbs and body .
492
LUMPY
Fig.
5.
SKIN
DISEASE
A limb swollen as a result of ISD infection.
Pneumonia is a common and often fatal complication of LSD. I,esions may be found throughout the upper respiratory tract and focal or larger areas of grey consolidation may develop in the lungs together with larger areas of bronchopneumania. Inhalation is a sequel of the necrotic lesions in the respiratory tract and it may prove f’ntal even months after the initial infection when a necrotic slough 1947). The pneumonias rarel, OCCL~ from an old tracheal lesion (de Boom, rrspond to antibiotic therapy. Xhortion frequently follows the acute infection in females, and infertility has been a problem in the months succeeding an outbreak. Bulls may have painful lesions of their genitalia, which can prevent them serving, and may remain infertile for 3-6 months after the disease. Females mav be anoestrous for se\~ral months. These effects are thought to he a consequence of the serious loss in COIIdition associated with LSD. Fetuses may be aborted, or the skin of calvrs t,orlI after an epi/ootic may be covered with lesions of ISD (Davies, unpublished data). Such intrauterine infections have also been described with swinepox ( BOI-st r/ (I/., 1990). Extensive skin lesions which produce a hidehourld condition, limb oedema and mouth and respirator-v lesions mav cause a prolonged anorexia and disinclination to I~OVC~. Rapid dete&ration in body condition follows and, LII~~CIrange COIIditions, the illability to move to water results in a higher mortality from dehvdration and predators. Some cattle become so emaciated that euthanasia is indicated.
