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Bulgarian Journal of Veterinary Medicine, 2024, 27, No 2, 254272
ISSN 1311-1477; DOI: 10.15547/bjvm.2022-0021
Original article
EPIDEMIOLOGY, DIAGNOSIS AND CONTROL OF LUMPY
SKIN DISEASE IN EGYPTIAN RUMINANTS
M. H. KHAFAGI, A. A. GHAZY & M. ABD EL-FATAH MAHMOUD
Parasitology and Animal Diseases Department, Veterinary Research Institute,
National Research Centre, Dokki, Cairo, Egypt
Summary
Khafagi, M. H., A. A. Ghazy & M. Abd El-Fatah Mahmoud, 2024. Epidemiology, diagno-
sis and control of lumpy skin disease in Egyptian ruminants. Bulg. J. Vet. Med., 27, No 2,
254272.
Lumpy skin disease (LSD) is one of the most important diseases causing great economic losses in live
animals stock industry of affected countries. It is an infectious vector borne viral illness considered
one of major trans-boundary animal diseases affecting cattle and Asian domestic buffaloes (Bubalus
bubalis). The aim of the current review is to clarify the current status of LSD epidemiology and to
throw light on the methods of LSD diagnosis, prevention, treatment and control. LSD is rarely fatal,
characterised by nodules on the entire skin of the affected animals, and has a high morbidity rate. The
disease has severe direct adverse effects on cattle production, milk yields and animal body condition
from damage of hides, abortions, infertility and other indirect effects resulted from restriction of ani-
mal movements and trade. The first recorded outbreak was in Zambia in 1929. It is considered an
endemic disease in African continent. First report of LSD in Egypt was in Suez Canal governorate in
1988. Diagnosis of LSD virus depends on the highly characteristic clinical signs in severely infected
cases. In mild cases the diagnosis depends on the detection and isolation of the virus on different cell
lines and on chorio-allantoic membranes of embryonated chicken eggs. Viral nucleic acid detection
by molecular techniques as real time PCR is considered the test of priority because it is rapid, sensi-
tive and quantitative. Prevention of the disease depends mainly on vaccination programmes for the
entire cattle and buffalo populations, restriction of animals’ movement inside the country and through
country borders, controlling insect vectors, in addition to symptomatic treatment of infected animals.
Key words: control, diagnosis, epidemiology, lumpy skin disease, ruminants
INTRODUCTION
Lumpy skin disease (Pseudo-urticaria,
Neethling disease, exanthema nodularis
bovis, and knopvesiekte) are multiple
names for one of the vector borne diseases
of cattle and Asian water buffaloes. Af-
fected animals suffer from fever, multiple
firm well circumscribed deep-seated skin
nodules and necrotic plaques in the mu-
cous membranes of the oral cavity and
upper respiratory tract, mastitis, and or-
chitis with generalised lymphoadenopathy
(Sprygin et al., 2019b). Although LSD is
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 255
of low mortality rate, the disease is of
major economic importance due to pro-
duction losses from severe emaciation,
drop in milk production, abortions, secon-
dary mastitis, loss of fertility, and hides
damage (Gari et al., 2011). It was first
reported in Northern Rhodesia in 1929
(Morris, 1930) and it was suggested that
the skin lesions resulted from insect bites
or plant poisoning. LSD was firstly de-
scribed as an infectious disease in 1943
after an epizootic in Northern Botswana
(Von Backstrom & Ngamiland, 1944).
LSDV is one of the capripoxviruses which
include lumpy skin disease virus (LSDV),
sheep pox virus (SPPV) and goat pox
virus (GPPV), in subfamily Chordopox-
virnea, family Poxviridae. Those capri-
poxviruses are responsible for great eco-
nomic losses of domestic ruminants in
Africa and Asia (Tuppurainen et al.,
2017a). From Central and East Africa, the
disease rapidly spread in Africa and was
first recorded in Ethiopia in 1983
(Mebratu et al., 1984). LSD was reported
as an endemic disease in Africa. The first
report of LSD in Egypt was in 1988 after
starting the importation of cattle from
African countries (House et al., 1990). It
was reintroduced in Egypt during 2006
and many outbreaks were recorded after
that in 2011, 2014, 2017, and 2018 (Salib
& Osman, 2011; Abdallah et al., 2018).
Although LSDV is transmitted mechani-
cally or biologically by arthropod vectors,
transmission can also occur through con-
sumption of contaminated food or water,
direct contact, contaminated semen in
natural mating and artificial insemination
(Abdulqa et al., 2016; Alkhamis &
VanderWaal, 2016). Severe cases of LSD
have characteristic clinical signs, but early
and mild cases of the disease need labora-
tory confirmation (Tuppurainen et al.,
2018). Real time PCR is the test of choice
for the viral nucleic acid detection, as it is
rapid, quantitative, simple, specific and
sensitive and can be used in large scale
testing (Sprygin et al., 2019a). LSD is
considered a major transboundary animal
disease due to its economic impact on
animal production, it is rapidly spread
across national borders resulting in inter-
national trade restrictions. Thus, regional
cooperation in prevention, control and
eradication including regular vaccination,
restricted animal movement and quaran-
tine, slaughter of infected animals, proper
disposal of contaminated materials and
disinfection of contaminated premises are
necessary (Gumbe, 2018). Therefore, this
review will throw light on LSD recent
situation updates raising concerns about
biology of lumpy skin disease virus,
mechanism of the disease spreading, clini-
cal and laboratory diagnosis and measures
for control and/or eradication.
BIOLOGY OF LSDV
Agent characteristics
LSD virus is a member of family Poxviri-
dae that includes the biggest viruses caus-
ing disease naturally in most domestic
animals except in dogs. It composed of
two subfamilies; Chordopoxvirinae, Pox-
viruses of vertebrates and Entomopox-
vivinae, Poxviruses of insects (Haegeman
et al., 2021). All capripoxviruses are gro-
wing slowly on cell cultures and may need
several passages on cells of bovine and
ovine origin. Intra-cytoplasmic eosino-
philic inclusion bodies can be seen micro-
scopically after staining the infected
monolayer cells with haematoxylin and
eosin (Prozesky & Barnard, 1982). The
virus causes macroscopic pox lesions
when propagated onto the chorio-allantoic
membranes of embryonated chicken eggs
(Hala et al., 2021).
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
256
Phylogenetics
The family Poxviridae is characterised by
its large and complex genome containing
single, linear molecule of double-stranded
DNA (dsDNA) coding for about 200 pro-
teins. DNA molecule is continuous with-
out free ends because the dsDNA are
ligated to each other (Toplak et al., 2017).
Poxviruses are the only DNA viruses that
complete their replication cycle in the
cytoplasm. In the cytoplasm, the produced
mRNA is translated to proteins and then
to copies of genome for progeny virions.
The new progeny virions are released
from the cell by budding. The Poxviridae
family has at least ten major antigens with
a common nucleoprotein antigen which
causes the cross-reactivity among species.
Ten viral enzymes are present within the
virus particles. Their function is to pro-
mote nucleic acid metabolism and genome
replication (Tulman et al., 2001; King et
al., 2012). Capripoxviruses include
LSDV, SPPV and GPPV. Their dsDNA
have around 150 kilo base pairs (Kbp)
and are relatively large in size (230260
nm). Their capsid containing the genome
and lateral bodies is brick or oval shaped.
There is extensive DNA cross hybridisa-
tion between species responsible for sero-
logical cross reaction and cross protection
between their members (King et al., 2012;
Calistri et al., 2019). They are sharing
about 97% sequence identity (Tulman et
al., 2002). Molecular studies indicated
that LSDV is phylogenetically distinct
from SPPV and GPPV as it has two
unique genes not present in sheep pox or
goat pox viruses (Tulman et al., 2002).
All available data suggest that there is
only one serotype of LSDV (Neethling
strain) as complete genome sequencing of
recent isolates of LSDV show 99.5% and
99.8% homology, respectively with the
field LSDV isolated in South Africa that
is ensuring genetic stability of LSDV and
indicate that the virus is a single serotype
(Toplak et al., 2017). The phylogenetic
analysis of G-protein coupled chemokine
receptors (GPCR) genes of LSD in cattle
and buffaloes in Egypt during the summer
in 2011 revealed that GPCR genes were
genetically closely interrelated showing
the ability of transmission of cattle LSDV
to water buffaloes (El-Tholoth & El-
Kenawy, 2016).
Virulence
So far, researches have not found differ-
ences in the virulence between different
LSDV isolates. The severity of the disease
is attributed mainly to the immune status,
breed, production stage and age of the
affected animals (Badhy et al., 2021).
Resistance and survival of the virus
LSDV is highly stable for long periods at
room temperature especially in air dried
hides. It is recovered for about 18 days,
33 days or longer and persists in necrotic
skin nodules, while in desiccated crusts
the virus remains viable up to 35 days.
The virus persists for several months in
contaminated animal sheds. Inactivation
of the virus can occur at temperature of
55 oC for two hours and 65 oC for 30 mi-
nutes. Also, it is stable at skin nodules at
80 oC for 10 years and in infected tissue
culture fluid at 4 oC for 6 months. Con-
cerning the stability of LSDV, it is suscep-
tible to high alkaline pH or acid pH and
stable at pH 6.68.6 for 5 days at 37 oC.
The virus is greatly susceptible to ether
(20%), chloroform, formalin (1%), phenol
(2%) for 15 min, sodium hypochlorite
(23%), iodine compounds (1:33 dilution)
and quaternary ammonium compounds
(0.5%) (OIE, 2017).
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 257
EPIDEMIOLOGY
Geographical distribution
LSD virus is causative agent of an en-
demic windy spread disease in Africa ex-
cept Algeria, Morocco, Tunisia and Libya.
The Americas and Australia are free from
all capripoxvirus infections (FAO, 2017).
In 2013, it was recorded in Turkey
(Timurkan et al., 2016) and now it is en-
demic in this country, its spread causing
many outbreaks in European countries
since 2014.
African first LSD report was in Zam-
bia, 1929 (Gari et al., 2011). In 1989,
LSD was recorded outside Africa through
Israel to Palestine, Jordan, Lebanon, Ku-
wait, Saudi Arabia, Iraq, Oman, Yemen,
United Arab Emirates and Bahrain
(Abutarbush et al., 2015; Al-Salihi &
Hassan, 2015; Sameea et al., 2017). It was
reported in the middle and east of Europe
in 2014 (Tageldin et al., 2014; Sameea et
al., 2017). In 2016, LSD was confirmed in
South East Europe in the Balkans and
Caucasus (OIE, 2017).
In Egypt, LSD was reported in 1988
after importation of cattle from Ethiopia
and other African countries where it was
clinically demonstrated in Suez Canal
governorates in the summer season of the
same year. The infection was not recorded
in the winter season (Ahmed et al., 2021).
In 1989, reoccurrence of LSD in a period
of five to six months was recorded within
22 of the 26 Egyptian governorates. In
summer of 2006, other outbreaks reoc-
curred in many of the Egyptian gover-
norates ( Abdallah et al., 2018). The reoc-
currence of the disease in Egypt after its
absence for 17 years was attributed to a
combination of the uncontrolled animal
movements, immune status of the animals,
wind and rains which are the most impor-
tant influences on the vector population
density and strengthen the transmission
rates (Al-sabawy et al., 2020). This was
followed by other outbreaks in 2011, 2014
and 2017 which may have occurred as a
result of the endemic status of the disease
when the virus finds its way to the non-
immune cattle herds. In 2017, the out-
breaks of LSD occurred though the impor-
tation of cattle from Ethiopia as a result of
the unlimited movement of animals at
country borders which is the major threat
for LSD (Zeedan et al., 2019). It was fol-
lowed by another outbreak in 2018-2019
that occurred mainly in the Nile delta and
the western region.
Host range
Cattle and Asian water buffaloes (Bubals
bubalis) are the main natural host to
LSDV with all ages and sexes susceptible
to infection, while calves develop severe
lesions 2448 hours earlier than their
dams (Elhaig et al., 2017). More severe
disease signs were recorded in thin skin
breeds as Friesians and in cow’s peak
lactation (Şevik & Doğan, 2017). No epi-
demiological data on the role of small
ruminants as a reservoir for LSDV have
been recorded although mixed herds of
cattle, buffaloes, sheep and goats are more
commonly encountered (Elhaig et al.,
2017). In Egypt, the LSDV is causing
unapparent to severe disease in native
breeds of all ages affected but severe
cases were found in young calves and
foreign breeds (Salib & Osman, 2011).
Also, isolation of LSDV from naturally
infected water buffaloes has a great role in
the appearance of disease outbreaks
(Elhaig et al., 2017; Sharawi & Abd EL-
Rahim, 2011). Although in another study
buffaloes were in contact with clinically
infected cattle confirmed by virus isola-
tion and PCR, none of buffaloes were
positive for LSDV by virus isolation and
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
258
PCR, despite little increase in antibodies
levels against LSDV in their sera (Elhaig
et al., 2017). Clinical signs of LSD have
been reported in Arabian Oryx (Oryx leu-
coryx) and spring box (Antidorcas marsu-
pialis). Also giraffe (Giraffa camelopar-
dalis) and impala (Aepyceros melampus)
have been experimentally infected, but
wildlife has no significant role in the epi-
demiology of the disease (Gortázar et al.,
2021). Experimental infection of sheep
and goats with LSDV can occurred, but
there is no natural infection with the virus
(Wolff et al., 2020). LSD is not a zoono-
tic disease (Şevik & Doğan, 2017).
Morbidity and mortality
Morbidity rates range from 10 to 20%
(OIE, 2021), but under certain conditions
may reach 8090% while mortality rate is
from 1 to 5% (Kiplagat et al., 2020). In
Egypt, morbidity rate recorded during
LSD outbreaks may attain up to 100%,
while mortality rates and case fatality in
Egyptian cattle: 1.8% and 1.8%, respec-
tively. The morbidity rate is high as a re-
sult of the exposure of cattle at the same
time to the infection with FMDV, which
has an immune suppressive effect and
theoretically could occur (OIE, 2017).
Transmission
Source of infections
The main source of LSDV infection to
healthy animals are clinically ill animals
whereas skin lesions are source of the
virus for a long period of time (Şevik &
Doğan, 2017). LSDV was also detected in
blood, nasal and conjunctival secretions,
saliva, semen and milk. In affected rumi-
nants, nodular lesions on different mucous
membranes (eye, nose, mouth, rectum,
udder and genitalia) may ulcerate and act
as a source of the virus (Tuppurainen et
al., 2015; Abdulqa et al., 2016). Viraemic
animals act as a source of infection as
viraemia may extend for up to two weeks
(Gari et al., 2011; Tuppurainen et al.,
2017a). The susceptible ruminants get
infected by blood feeding arthropods (bi-
ting flies, mosquitoes and ticks), through
direct contact or contaminated feed and
water in seldom cases. Intrauterine trans-
mission can occur at late gestation and in-
fected cows deliver calves exhibiting skin
lesions all over their bodies with immature
developed signs, they may die within few
hours after birth (Rouby & Aboulsoud
2016). Calves are infected either through
LSDV-contaminated milk or from teats
lesions (Sprygin et al., 2019b). Accidental
transmission may happen during mass
vaccination with a single syringe, in this
case the needle spreads virus from skin
lesions or viraemic animals to healthy
ones (Tuppurainen et al., 2017b).
Route of transmission
Direct transmission. Direct contact does
not have an efficient role in LSDV trans-
mission (Sprygin et al., 2019b), but some-
times it may have a respective role in
LSDV transmission as outbreaks of the
disease are reported in absence of the in-
sect vectors (Sprygin et al., 2019b).
Transmission via semen is experimentally
reported (Abdulqa et al., 2016). During
experimental infection, live LSDV was
isolated from semen 42 days post infec-
tion (dpi) and specific viral DNA was
demonstrated using PCR 159 dpi from
bulls that showed no clinical signs (Irons
et al., 2005). Vaccinated bulls with Neeth-
ling LSDV strain didn’t shed vaccine vi-
rus in their semen (Osuagwuh et al.,
2007).
Indirect transmission. Earlier studies
suggested that LSDV transmission bet-
ween naive (non-immune animals) and
infected animals kept together failed in
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 259
transmission of the virus (Sprygin et al.,
2019b), but recent experimental studies
suggested that 50% of these animals pre-
sent clinical signs and others are only vi-
raemic (Sohier et al., 2019; Wolff et al.,
2020). Further studies are required for
clarifying the LSDV transmission mecha-
nisms. Recent data about the occurrence
of LSD in Russia found infected cases 800
km away from the centre of the outbreak
which was attributed to the use of the
same vehicles that transport infected ani-
mals (Sprygin et al., 2019b).
Role of vectors
It has been ensured that large populations
of arthropod vectors have a good chance
to carry and transmit the virus. These vec-
tors vary according to geographical re-
gions (Alkhamis & VanderWaal, 2016).
There are no biological arthropods vectors
for LSDV, mechanical role of transmis-
sion only occurs. High density of biting
arthropods affect the disease prevalence,
in the presence of warm and humid
weather conditions (Şevik & Doğan,
2017; Gumbe, 2018). There is a higher
prevalence of LSD recorded in wet sum-
mer and fall months in South Africa (Gari
et al., 2012). In Egypt, LSD outbreaks
were reported in summer and fall seasons
in the presence of insect vectors that have
a main role in virus transmission and
which are abundant in these seasons,
while the disappearance of cases were
seen in winter (Salib & Osman, 2011).
Transmission between different herds that
keep long distance between each other
and the presence of quarantine measures
suggests that the infection is vector-
mediated as the disease outbreaks at dif-
ferent governorates of Egypt in summer
1989 occurred despite restrictions of ani-
mal movements (Fayez & Ahmed, 2011).
Also, high morbidities are observed where
mosquito population is abundant. Me-
chanical transmission through contami-
nated mouth parts of vectors is also possi-
ble (Sprygin et al., 2019b). Recently, so-
me researches concentrated on the role of
ticks carried by migratory birds in trans-
mission of LSDV (Sprygin et al., 2019b).
Molecular studies showed trans-ovarian
transmission of LSDV by Phipicephlus
decoloates ticks, Phipicephlus appen-
diculates and Amblyomma hebracum ticks
(Lubinga et al., 2014). Aedes aegypti has
been involved in airborne transmission
over long distance in free areas of disease
which complicates the control measures
by animal movement restriction (Sprygin
et al., 2019b). The virus has been also
detected in Stomoxys, Biomyia, Musca,
Culiciodes and Glossina species which
potentially transmit LSDV (Issimov et al.,
2020). A significant role of Culicoides
species was reported in the transmission
of LSDV during 20142015 in Turkey
(Şevik & Doğan, 2017). The wind cur-
rents play an important role in the spread-
ing of virus by female Culiciodes and
mosquitoes (Issimov et al., 2020). Severe
climatic changes in the three months be-
fore the epidemic outbreak have a role in
the spread of the disease, as happened in
Egypt in 1989 and 2006. In 1989, Occu-
pied Palestine was attacked by LSD out-
break and the source of the virus was from
the Egyptian Domiatta and Port Said gover-
norates (El-Sherif et al., 2010). Another
outbreak occurred in Nile delta, Suez Ca-
nal and North Sinai in 2006 due to impor-
tation of cattle from Ethiopia. The disease
spread to Occupied Palestine and Saudi
Arabia at the same time. Stable flies were
recorded to have a role in the wind trans-
mission of LSDV from Egypt to Occupied
Palestine (Calistri et al., 2018). All these
studies confirmed that infected vectors
have a great role in the transboundary
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
260
transmission of vector borne diseases in
the Middle East and Europe, as Middle
East is present in an area which joins
Europe, Africa, and Asia (Sprygin et al.,
2019b).
Pathway of the disease
The movement of animals is the main risk
factor to introduce infectious diseases into
disease-free areas. The pathway of LSD
introduction comprises introduction of
infected animals, movement of flying vec-
tors and the windborne transmission of
vectors carrying the LSDV in blood meal
from an infected animal (Şevik & Doğan,
2017). In 2014, epidemiological investi-
gations of LSD outbreaks in Egypt, Pales-
tine, Iran and Azerbaijan revealed that the
legal and illegal animal movements are
the pathway for LSDV introduction (OIE,
2017). The biggest movements of live
cattle in Muslim countries reach a peak on
Eid El-Adha which enhances the animal
trade of high numbers of animals. Such
movements of high numbers of animals
over a short period of time may have re-
sulted in poor regulation and increased
risk of introduction of the transboundary
animal diseases (Sprygin et al., 2019b).
DIAGNOSIS
Clinical diagnosis
Clinical signs
LSD incubation period in natural infection
ranges from 2 to 5 weeks, while in ex-
perimental infection: between 47 days
(Wolff et al., 2020). There are mild and
severe forms depending on the number of
nodules, susceptibility of the host, insect
population and occurrence of complica-
tions. LSD can be diagnosed clinically
depending on its highly characteristic
signs but mild and asymptomatic disease
is difficult to be demonstrated and rapid
laboratory techniques are needed to con-
firm the diagnosis (Tuppurainen et al.,
2005; Calistri et al., 2018). The signs be-
gin with fever over than 40.5 oC for about
one week with depression, anorexia and
sharp drop in milk production in dairy
cattle and lactating buffaloes (FAO, 2017;
Tuppurainen et al., 2017b). The character-
istic lumps (nodules) appear after 2 days
of fever. Their diameters range from 1 to
7 cm, they are uniform in size, painful,
inflamed and may be scattered all over the
animal body especially on muzzle, genita-
lia, udder, eyelids, ears, nasal and oral
mucosa where they may persist for 12
days. Hundreds of nodules can cover the
entire animal body involving all skin lay-
ers reaching the muscular layer. Then
nodules became moist, necrotic and ulcer-
ated (Sanz-Bernardo et al., 2020). After
persisting for a long time, the lesion ul-
cerates and scabs are formed on its top.
The lesions may involve large areas, ag-
gregating to form a hole through all skin
thickness which is called “Set Fast”
(Abutarbush et al., 2015). Affected ani-
mals demonstrate salivation, lacrimation,
nasal discharge and enlargement of super-
ficial lymph nodes (ten times their original
sizes). Complicated clinical signs lead to
mastitis, temporal or permanent sterility in
bulls and cows due to lesions on genital
organs, severe lameness caused by lesions
above the joints of the limbs. Keratitis is
also reported (bilateral or unilateral). Le-
sions in the respiratory tract are followed
by pneumonia (Babiuk et al., 2008). In
Egypt, mild form of LSD was recorded in
native breeds of cattle but severe form
was reported in foreign breeds (Salib &
Osman, 2011). During the LSD outbreak
in 2006 in Egypt, about 95% of caws had
no ovarian activity, no signs of estrus and
the ovarian size was smaller than normal
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 261
as detected by transrectal ultrasonography
examination (Ahmed & Zaher, 2008).
Recovery from infection is slow, the ne-
crotic skin area exposed to fly strike are
shed giving rise to deep holes in the hide
(OIE, 2017).
Post mortem findings
At the slaughterhouse skinned infected
animals show subcutaneous lesions. LSD
lesions are found in respiratory and diges-
tive tracts and on most of the internal or-
gans. Necrotic areas about 12 cm in di-
ameter are found, then scar formation oc-
curs weeks after acute stage (Sanz-Ber-
nardo et al., 2020).
Histopathological findings
Acute histopathological lesions include
epidermal vascular changes with intracy-
toplasmic inclusion bodies and vasculitis,
and chronic histopathological lesions
showing fibrosis (Sanz-Bernardo et al.,
2020). Histopathological findings of LSD
provide the basis of diagnosis. Ballooning
degeneration was found in the cell layers
of skin nodules and eosinophilic intracy-
toplasmic inclusion bodies specific for
LSD virus infections. Epidermal layer of
skin exhibits necrosis and large number of
neutrophils, lymphocytes and macro-
phages. The dermal layer is infiltrated
with inflammatory cells and the muscular
layer is necrotic. Aggregation of inflam-
matory cells around the blood vessels is
recorded (Salib & Osman, 2011; Cons-
table et al., 2017).
Haematological and biochemical changes
There is an alteration in biochemical
analysis results due to liver and kidney
failure and severe inflammatory changes
which occurred due to disease complica-
tions as anorexia and decreased muscular
mass during LSD infection (Abutarbush et
al., 2015; Neamat-Allah, 2015; Şevik et
al., 2016). Macrocytic hypochromic ana-
emia, leukopaenia, lymphopaenia, throm-
bocytopaenia, hyperfibrinogenaemia, de-
creased creatinine concentrations, hyper-
chloremia, hyperkalemia, decreased total
protein and albumin, increased globulins
were detected in sera of naturally infected
cattle (Abutarbush et al., 2015). Serum
biochemical analysis indicates increased
activity of aminotransferases, alkaline
phosphatase, globulins and creatinine
concentrations (Şevik et al., 2016; El-
Mandrawy & Alam, 2018).
Differential diagnosis
Severe cases of LSD give characteristic
clinical signs, but early and mild cases of
the disease need laboratory confirmation
(Tuppurainen et al., 2017b). Sometimes
the condition may be confused with foot
and mouth disease and bovine and malig-
nant catarrhal fever (Constable et al.,
2017).
Laboratory diagnosis techniques
Post-mortem examination is not com-
monly carried out in the field, by reason
of the highly characteristic clinical signs
in severely infected cases of LSD and the
fact that mild infected cases don’t show
internal lesions. So it is preferred to take
samples from live animals for laboratory
diagnosis (FAO, 2017). The most suitable
samples from live animals are skin nodu-
les, scabs, saliva, nasal secretions, and
blood for virus isolation, PCR detection of
LSDV and electron microscopy (FAO,
2017).
Virus detection (live virus or viral
nucleic acid)
Virus isolation
Live virus can be propagated on dif-
ferent bovine and ovine cell lines (primary
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
262
lung, kidney or testicle cultures). LSD
grows slowly on cell culture and needs
many passages to enhance its growing as
on VERO cell line and Baby Hamster
kidney cell line (Babiuk et al., 2008).
Egyptian isolates are able to replicate di-
rectly on chorio-allantoic membranes
(CAMs) of specific pathogenic free-
embryonated chicken eggs (SPF-ECE)
inducing small white foci spread on the
CAM, and also may result in their thick-
ening and congestion (El-Kenawy & El-
Tholoth, 2010; El-Nahas et al., 2011;
Hodhod et al., 2020).
The general CaPV real time PCR
methods
Molecular assays, gel-based PCR and
real-time PCR are very sensitive, well
validated and mainly used in detection of
the presence of capripoxviruses nucleic
acid (CaPV DNA) (Vidanovic et al.,
2016; Chibssa et al., 2018). The real time
PCR method used for detection of CaPV
has greater sensitivity than conventional
gel-based PCR assays; no cross reaction
with related poxviruses and no false posi-
tive results are reported. Real-time PCR is
rapid, quantitative, simple, specific and
sensitive. It can be used in large scale
testing ( Sprygin et al., 2019a). CaPV gel
based PCR is good choice if real time
PCR is not available as it is cheap and of
good sensitivity and specificity, but not a
quantitative technique (Chibssa et al.,
2018). Conventional PCR can also differ-
entiate between SPPV and GTPV
(Gnanavel et al., 2012; Mahmoud &
Khafagi, 2016; Zeedan et al., 2021).
Species-specific real time PCR
methods
Species-specific real time PCR meth-
ods are used for differentiation of capri-
poxviruses (SPPV, GTPV and LSD); they
can detect and differentiate these viruses
in EDTA blood, scabs, ocular and nasal
lesions, saliva and semen samples. The
species specific PCR assay recorded dif-
ferences in melting point temperature be-
tween probe and its target which will re-
sult in different melting temperature for
SPPV, GTPV, and LSD detected after
fluorescence melting curve analysis
(Chibssa et al., 2018).
Portable pen side PCR
Portable pen side PCR is a field test
showing result within one hour and there
is no need for cold chain. Its reagent is
freeze dried, quick confirmation enhances
efficacy of the control measures (Armson
et al., 2017). Also rapid recombinase po-
lymerase amplification (RPA) is 100%
sensitive when compared with real-time
PCR results which can be used in field or
at quarantine stations for LSD identifica-
tion (Cabada et al., 2017).
Loop-mediated isothermal
amplification assays (LAMP)
It is a molecular test that uses the loop-
mediated isothermal amplification for
identification of capripoxviruses genomes
recording the same sensitivity and speci-
ficity like real-time PCR, but the latter is
more simple and of low coast (OIE,
2017). Interpretation of LAMP results
depends on colour changes, its sensitivity
ranges from 70100% and the specificity
ranged within 92.3100% (Mwanandota
et al., 2018).
Gene sequencing
Sequencing of host range genes re-
quires well trained staff and expensive
equipment but it can detect the virus
(Sprygin et al., 2019b). It is considered as
an important technique in molecular epi-
demiology analysis of the LSD for differ-
entiation of virulent isolates which are
highly conserved compared with vaccinal
isolates by complete genome sequencing
(Menasherow et al., 2014; Gelaye et al.,
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 263
2015; Saltykov et al., 2021) or by RP030
phylogenetic analysis of different isolates
(Molini et al., 2018).
Electron microscopy
It needs expensive specialised and
trained staff and cannot even differentiate
Capripox from Orthopox virus members
(Sprygin et al., 2019b).
Detection of antibodies against LSDV
LSDV host immunity depends on cell
mediated immunity rather than on hu-
moral immunity. Low antibody titres in
mild infection and/or vaccinated animals
cannot be sensitively detected (Gari et al.,
2011; Tuppurainen et al., 2017b).
Serum virus neutralisation test
It is the gold standard serological
technique yet it cannot detect low anti-
body titres in LSD infected animals. Its
sensitivity ranges from 7096% and the
specificity may reach 100% (Babiuk et
al., 2008).
Indirect fluorescent antibody test
(IFAT)
The capacity of the assay permits test-
ing larger number of samples than the
neutralisation test. It can be used to evalu-
ate immune status against LSDV in epi-
demiological studies (Gari et al., 2008;
2011).
Agar gel immune diffusion test
(AGID)
AGID is a simple test of low sensiti-
vity, its results must be confirmed with
another test (Sprygin et al., 2019a).
Enzyme linked immunosorbent assay
(ELISA)
ELISA IDVet was the first validated
ELISA assay. It is commercially available,
and facilitates large-scale serosurveillance
for LSD. While the VNT is labour inten-
sive and needs more time, it is the test
recommended by the OIE (Krešić et al.,
2020). VNT has a higher specificity than
ELISA (Samojlović et al., 2019).
Western blotting
Western blotting used in detection of
antibodies in sera against capripoxvirus
infected cell lysate is considered a specific
and sensitive system for detection of ca-
pripoxviruses structure protein antibody,
but is expensive and labourous (OIE,
2017). Its difficulty is due to requirement
for pure antigens, also it is not easy to
perform. Western blotting is used mainly
as a confirmatory test to verify SNT and
ELISA positive results (Sprygin et al.,
2019b).
CONTROL OF LSD IN ENDEMIC
COUNTRIES
Egypt had recent outbreaks due to several
factors including its geographical position
between three continents: Africa, Asia and
Europe, political events with adverse im-
pact on regional cooperation, the great
differences in climatic conditions between
different regions, the uncontrolled animal
movement, import of animals and animal
products, routes of migratory birds be-
tween Africa and Europe, increasing hu-
man population and water resources limi-
tation. All these factor badly affect LSD
control plans (Shimshony & Economides,
2006). For minimising LSD losses, con-
trolling measures include regular vaccina-
tion (Wallace et al., 2020), restricted ani-
mal movement and quarantine, discarding
of affected animals, proper disposal of
contaminated materials and disinfection of
contaminated premises (Şevik & Doğan,
2017). Finally, prevention in endemic
countries with LSDV infection as Egypt
and most of the African countries, de-
pends mainly on vaccination and suppor-
tive symptomatic treatment of infected
animals (Wallace et al., 2020).
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
264
Prevention
Controlled vaccination programmes to the
entire cattle and buffalo population should
be implemented, restricted movement of
ruminants inside the country and across
country borders as movement must be
authorised. Vaccinated animals movement
must be restricted until full immunity
reached (28 day after vaccination). Insect
repellents and insecticides should be regu-
larly used to reduce the vector-borne
transmission of the disease and the risk of
disease spreading by this route of trans-
mission (FAO, 2017). Cleaning and disin-
fection on infected farm premises with
removal of dirt and manure should be
practiced (FAO, 2017). Vaccination is the
only effective method to control the dis-
ease in endemic areas as movement re-
strictions and removal of affected animal
alone are usually not effective (Tuppu-
rainen et al., 2017b; Mulatu & Feyisa
2018; Namazi & Tafti 2021). In addition,
rapid confirmation of a clinical diagnosis
is essential so that eradication measures
such as quarantine, slaughter-out of af-
fected and in-contact animals, proper dis-
posal of carcasses, cleaning and disinfec-
tion of the premises and insect control can
be implemented as soon as possible dur-
ing eruption, moreover rigorous import
restrictions on livestock are important
(Constable et al., 2017; Tuppurainen et
al., 2017a).
Immune response
Capripoxviruses (CaPVs) differ from
other enveloped viruses, because the most
predominant immunity type produced in
infected animals is cell mediated immu-
nity (Hamdi et al., 2021). Naturally this
occurs as a result of the nature of CaPV
which remain inside infected cells. They
spread from cell to cell (Tuppurainen et
al., 2021) so the immune status of previ-
ously infected or vaccinated animals
should not be estimated by the level of
serum neutralising antibodies (Kitching &
Smale 1986). All CaPV are sharing com-
mon antigens and thus these viruses ex-
hibit immunological cross reaction (Gela-
ye et al., 2015; Molini et al., 2018). Ap-
parent or unapparent natural infection
with LSD gives up to 3 log of neutralising
antibodies against the virus. This level of
immunity protects well the animal from
reinfection for its whole life (Milovanović
et al., 2019). Vaccinated animals develop
low antibody titres against LSDV, begin-
ning within 15 days post vaccination and
reaching peak level after 30 days
(Samojlović et al., 2019). Some vaccina-
ted animals are fully protected without
seroconvertion occurring (Smith &
Kotwa, 2002; Ayelet et al., 2013).
Vaccination strategy
LSD control is depending mainly on vac-
cination which is the main effective
method for control as restriction of
movements and culling of affected ani-
mals are not effective alone to control the
disease. Objective of vaccination in en-
demic areas is rather clinical protection
than elimination of the virus circulation
(Calistri et al., 2018; 2019). Vaccination
of susceptible cattle and buffaloes should
be done annually. Stopping of vaccination
in the inter epidemics periods is the great-
est problem facing the control of LSD
recurrent outbreaks (OIE, 2017; Mulatu &
Feyisa, 2018). Only live vaccines against
LSD which are authorised for use in rumi-
nants in Africa to reduce the economic
losses from LSD are now available.
Eighty percent vaccination coverage in
cattle helps to cut the virus transmission
cycle and gives good protection from re-
current outbreaks (Tuppurainen et al.,
2017a). Recurrent outbreaks recorded in
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 265
Turkish animals resulted from insufficient
vaccination coverage (Calistri et al.,
2019). Calves from non-immunised dams
can be vaccinated at any age, while calves
from infected or vaccinated dams should
receive the vaccine at 36 months of age.
Regional vaccination should be done be-
fore animals’ movement (OIE, 2017).
Available LSD vaccines
Commercially available live attenuated
strains of capripoxviruses are used for
vaccination in order to control LSD (OIE,
2017).
Attenuated sheep pox and goat pox
vaccines
These vaccines are used in countries
where LSDV, SPPV and GTPV are pre-
sent. Kenyan sheep and goat pox viruses
by 18 passages in lamb testis (LT) cells or
foetal calf muscle cells, Yugoslavian
RM65 sheep pox strains and Romanian
sheep pox strain used in vaccination of
susceptible animals in Egypt are prepared
by 60 passages on Lamb kidney cells and
20 times passages on chorioallantoic
membrane of embryonated chicken eggs
(Hamdi et al., 2021). The vaccine dose
(0.5 mL by intradermal route in the tail
fold of cattle over 6 month of age) could
give a 3-year protection. Insufficient pro-
tection from sheep and goat pox based
vaccine was recorded in Turkish animals
especially when the dose of the vaccine
was less than 10 times the amount given
to sheep (Calistri et al., 2019). The partial
protection from these vaccines against
LSD will be effective if there is full vac-
cination coverage and restricted move-
ment control measures (Tuppurainen et
al., 2017b). Partial protection of the vac-
cine in vaccinated animals was noticed in
Egypt in summer 2016 and 2017, where
LSD symptoms were seen in 5% of cattle
previously vaccinated with the Romanian
SPPV vaccine, previously noticed in out-
breaks of LSD in Ethiopia among cattle
vaccinated with sheep and goat pox vac-
cine (Kenya Strain KS) due to lack of
LSDV antibodies protection and lake of
cross protection (Lubinga et al., 2015;
Zeedan et al., 2019). Evaluation of the
vaccine efficacy under field condition
must be qualified (Abdallah et al., 2018).
Homologous live attenuated LSDV
vaccine (Neethling strain)
It is effective in prevention of infec-
tion about four times more than the 10-
fold dose of Romanian strain sheep pox
vaccine (RM. 65 SPPV) (Ben-Gera et al.,
2015; Sprygin et al., 2019b). This vaccine
is allowed for use by the Egyptian veteri-
nary authorities for vaccination of cattle
and buffaloes livestock in Egypt since
2019, and now is produced by Sera and
Vaccine Research Institute, Egypt and
seems to give a complete protection
against LSDV infection for about 3 years
in cattle, including small calves and preg-
nant cows.
Adverse reactions of available
vaccines
Mild adverse reactions may be showed
in 0.09% of the vaccinated animals with
attenuated LSDV vaccines, called Neeth-
ling disease (Ben-Gera et al., 2015),
which including fever, low drop in milk
production and superficial small lesions
may appear at 7-17 days post vaccination.
These signs disappeared within 23 weeks
without any complications into necrotic
scabs or ulcers (Tasioudi et al., 2016;
Agianniotaki et al., 2017; Abutarbush et
al., 2015 and (Tuppurainen et al., 2017a;
Katsoulos et al., 2018). Full protection is
occurred about three weeks post vacci-
nation. During these three weeks vacci-
nated animals may be infected by field
virus and show clear clinical signs. Others
may be in incubation period at the time of
Epidemiology, diagnosis and control of lumpy skin disease in Egyptian ruminants
BJVM, 27, No 2
266
vaccination and thus give rise to clinical
signs less than ten days after vaccination
(FAO, 2017).
Animal movement control
The movement of unvaccinated animals
during LSD outbreaks is an important risk
factor. Strict regulation on the movement
must be applied by veterinary authorities.
Cattle must be vaccinated before moving
for at least 28 days, also unvaccinated
animals should not allowed to move dur-
ing outbreaks. Open transport vehicles
give time to insect vectors to transmit the
virus from cattle moving to slaughter-
houses which must be in restricted zones
(FAO, 2017; OIE, 2017). The OIE guide-
lines advised 3 km protection ring zone
from infected herd or village, 20 km zone
for surveillance and at least 50 km restric-
tion zone around the outbreaks area (OIE,
2017). Recent reports allow vaccination
zone of at least 50 km in radius around
infected area and at least 90% vaccination
coverage (FAO, 2017).
In many countries in Africa there are
no quarantine measures, there is no clear-
ance between these countries and an inter-
national organisation for control and pre-
vention of infectious diseases (Shimshony
& Economides, 2006). The lack of infor-
mation and notification about the diseases
to prevent the effect on the international
trade, lack of laboratory capacity which
affects the early reporting of disease, are
problems faced by us in controlling and
preventing infectious diseases including
LSD (Abutarbush et al., 2015).
Treatment
The treatment strategy depends on the
enhancement of the animal immunity.
This can be achieved by use of plant-
derived compounds such as curcumin,
resveratrol, epigallocatechol-3-gallate, qu-
ercetin, colchicine, capsaicin, androgra-
pholide and genistein (Jantan et al., 2015).
The second step of the treatment is the
antimicrobial treatment in animals with
clinical signs of LSD and complications to
overcome the secondary bacterial infec-
tions and save the animal life. Terramy-
cin® long acting oxytetracycline could be
used by the intramuscular route at a dose
of 1 mL/ 10 kg body weight. In addition,
subcutaneous injection with 10 mL leva-
mizole per animal acts as immunostimu-
lant drug. Intravenous injection of metam-
izole (Novacid®) at 20 mL/animal twice
daily until recovery from fever and once
daily intramuscularly after that may be
applied. Diclofenac sodium can be admin-
sitered for fever resolution (Salib & Os-
man, 2011).
CONCLUSION
LSD is an infectious disease of cattle and
buffaloes, causing great losses in non-
immune and young animals from reduc-
tion in weight and milk production, gene-
ralised skin lesions and loss of hide, infer-
tility, abortion and mortalities. LSDV
remains viable for 15 day post infection in
ocular and nasal discharges, in scabs for 6
months and in air dried hides for about 18
days. Arthropod vectors have an impor-
tant role in LSDV transmission between
susceptible animals by mechanical route.
Direct and indirect contact are possible
routes for LSDV transmission. The
movement of diseased animals and ar-
thropods vectors is the main possible
pathway for LSD introduction, windborne
transmission of vectors (after blood meal
from infected animals) represents an im-
portant route of LSD introduction into a
country. Movement of animals across
boundaries of countries should be re-
stricted and authorised.
M. H. Khafagi, A. A. Ghazy & M. Abd El-Fatah Mahmoud
BJVM, 27, No 2 267
Rapid reliable laboratory confirmation
is important for early diagnosis and con-
trol of disease spread. Real time PCR is
the method of choice for diagnosis of
LSDV infection. Only live attenuated vac-
cines against LSD are commercially avail-
able. Romanian strain of sheep pox vac-
cine cannot give effective protection
against LSD. Neethling attenuated LSDV
vaccine should be taken annually and not
neglected between outbreaks periods.
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Paper received 04.03.2022; accepted for
publication 18.06.2022
Correspondence:
Mohamed Abd El-Fatah Mahmoud
Parasitology and Animal Diseases Department,
Veterinary Research Institute,
National Research Centre, Dokki,
Cairo, Egypt
email: m_elfatatri@yahoo.com
ORCID: 0000-0001-9606-4022
