An Outbreak of Lumpy Skin Disease in a Holstein Dairy Herd in Oman: A Clinical Report
Somasundaram Mathan Kumar
Lumpy Skin Disease (LSD) is an acute infectious disease of cattle with significant economic importance and endemic in Middle East and Africa. LSD re emerge once again in this decade as an important threat to livestock health and dairy industry in Middle East by repeated out breaks. This clinical report aimed to register one such LSD outbreak that occurred in 2009 in Oman in a farm population of 3200 Holstein animals. This manuscript will be the first one to report LSD occurrence in a multiple thousand Holstein cattle population, till date no LSD outbreaks were reported with such a high numbered population either in the region or around the world where farm as an epidemiological unit. In contrast to the field outbreaks, this farm LSD incidence had a high mortality of the adult herd (12%). Herd milk production dropped by 40-65% and production loss continued for few months. Control measures against LSD like eradication of both affected population and contact population, control of vectors were not feasible with this herd outbreak. Vaccination was conducted in the wake of outbreak and yielded poorer results. Treatment outcome of the affected animals was poor and recovery was typically complicated by higher ambient temperature. Source of vector to this catastrophic episode remains inconclusive. In conclusion, manuscript emphasizes the need for further epidemiological and entomological studies at a national level in Oman.
Received: January 07, 2011;
Accepted: April 26, 2011;
Published: June 29, 2011
Lumpy Skin Disease (LSD) is an acute infectious disease of cattle which is
characterized by high fever, lymphadenopathy, sudden eruption of multiple circumscribed
skin nodules, necrotic plaques in mucosa and subsequent sit fasts of the nodules
(Woods, 1988). LSD is caused by prototype strain of
Neethling virus and belongs to the genus Capripoxvirus within the family
Poxviridae. Sheep Pox Virus (ShPV), Goat Pox Virus (GPV) and Lumpy Skin Disease
Virus (LSDV) together make up the Capripox group of pox viruses (Buller
et al., 2005). The morbidity of LSD varies from 3 to 85% and mortality
never exceeds 3% (Woods, 1988; Barnard
et al., 1994). However, severity of the disease depends on the susceptibility
of the host. By natural predisposition Bos Taurus is more susceptible
than Bos Indicus and lactating cows appearing to be at most risk (Davies,
1982; Kitching, 2008). LSD is a constraint on livestock
trade as it causes major production losses notably in high-producing exotic
breeds (Davies, 1991). This is an OIE (Office International
des Epizooties) listed and a notifiable cattle disease. LSD is signified with
the potential for rapid spread and is known to cause severe economic losses
by loss of milk production, abortions and infertility in males and females (Irons
et al., 2005; OIE Animal Diseases Data, 2011).
Until the 1980s, LSD was found only in sub Saharan Africa. In Middle East,
outbreaks were reported in Oman in 1984, Kuwait in 1986 and 1991, Egypt in 1988
and 2006, Israel in 1989 and 2006, Bahrain in 1993 and 2002-2003 and United
Arab Emirates in 2000 (USDA-APHIS Info Sheet, 2006; Brenner
et al., 2006; El-Kholy et al., 2008).
Epidemiological evidence indicates that biting arthropods such as Stomoxys
calcitrans and also female mosquitoes of Aedes aegypti are involved
in the transmission of LSDV (Kitching, 2008; Chihota
et al., 2001). Recent experimental evidence that concluded a potential
role of Ixodid ticks in the transmission of LSDV (Tuppurainen
et al., 2011).
Brenner et al. (2006) reported that LSD remerged
once again in Israel in June 2006 in an independent Holstein dairy herd. The
outbreak affected 30 cows in a 395 lactating group among the herd strength of
605 animals. Seemingly, this outbreak was considered as a serious threat to
the Israelian dairy industry as it concurred with a widespread Egyptian LSDV
outbreak (Brenner et al., 2006). Likewise, in
Oman re emergence of LSD in several regions within the country can be considered
as an emerging threat to the dairy industry. This communication is not intended
to be a comprehensive review of lumpy skin disease that occurred in several
regions of Oman in (2009). This clinical report is written out in the personal
perspective of veterinarian who handled this catastrophic episode and describes
clinical features of the herd outbreak. However, this independent episode clearly
raise an increased concern over LSD occurrence in intensively managed dairy
farms due to the fact, that Middle East region is prominently known for its
commercial dairy operations with multiple thousand populations of Holstein cattle.
The aim of the present study is to record a rare herd outbreak of lumpy skin disease in a multiple thousand Holstein farm population and describe the clinical features of this herd outbreak.
The Holstein herd is located in the Batinah region of Northern Oman and was operating with total herd strength of 3200 animals with a subset of 1250 milking cows. The farm is functioning nearly three decades and more than a decade as a closed herd. The farm operates under intensive management system, 3X milking, AI breeding and did not succumb to any other disease outbreak previously. The animals are housed at thirty three corrals and with corral cooling systems as fog/line sprinkler along with fans.
An independent cow was observed with severe lumpy/urticaria like lesions all
over the skin in the early morning of 2nd May 2009. Upon immediate screening
in an hour eight more cows were detected with similar signs and all were isolated.
Herd check and isolation continued on the next day, to realize 40 more cows
were suspected to be infected with LSD. The management was notified about this
sudden catastrophe and briefed the consequences. Whole herd vaccination was
conducted with KGSP 0/240 102.5 TCID 50- Kenya VacR (JOVAC,
Jordan Bio industries centre, Jordan) 1 mL/dose, subcutaneously on the third
day of outbreak. Clinical features were of characteristic lumps all over the
skin, persistent high pyrexia (40-41.5°C) and profound depression. (Fig.
1). Affected animals were observed with increased salivation, nasal discharge,
lacrimation anorexia and they were reluctant to move. The nodules were concentrated
at neck along with pre scapular lymphadenopathy (Fig. 2).
The disease continued to spread among all groups within the herd including the
young replacement stock (Fig. 3).
|| Large circumscribed lumpy nodules all over the skin
|| Characteristic LSD nodules in the neck along with prescapular
lymph node swelling
|| A yearling heifer with LSD
Majority of the affected population was observed with variable degree of lameness
that accompanied with edema of limbs (Fig. 4, 5).
Affected cows were noted with kerato conjunctivitis and corneal opacity (Fig.
6). As the disease progressed, the nodules become raw ulcers, on the mucous
membranes that coalesce to form a deep ulcer with severe necrosis (Fig.
7) and eventually forming a typical sit fast (Fig.
8). Extensive generalization of the disease was observed in most of the
affected cows. They became severely lame, recumbent in the terminal stages and
observed with severe tendosynovitis of the limbs (Fig. 9).
The whole disease episode lasted for 5-6 weeks since the start of May. Morbidity
of LSD in the herd was 30-35% and mortality of the adult herd was 12%. Until
end of two months total adult herd loss was 259 numbers that includes the adult
replacement heifers signifying the loss of future production stock.
|| Lameness and edema of LF limb
|| Lameness of RF and RH limb
|| Ocular discharge and corneal opacity
Upon necropsy, several ulcerative pox type lesions were noted in the upper
gastro intestinal and respiratory tract. A total of 13 abortions were occurred
as a direct loss of pregnancy. Recovering cows were noted with various degrees
of skin lesions such as deep ulcers, agalactia, emaciation, lameness and recumbency.
||Raw ulcers all over the skin in later stages
|| Typical sit fast and ulcers at the left nostril
|| Severe generalization of the disease and recumbency
Recovery of the affected herd was typically complicated by prevailed higher
ambient temperatures. The average temperature humidity indexes (THIs)
were of 90 and above during the summer months of June, July and August. Added
another 125 animals were died between July and August 2009 due to pronounced
loss of body condition and recumbency.
As mentioned above, characteristic clinical signs such as circumscribed nodules,
pyrexia, lymphadenopathy, necrosis of the nodules that later coalesce to form
ulcers, lameness, severe respiratory distress, extensive generalization of the
skin lesions and characteristic progressive stages of the lumps to sit
fasts (Fig. 1-9) all were consistent
with the presence of LSDV infection in the herd and a clinical diagnosis was
made. The scale of disease spread and characteristic clinical signs of LSD ruled
out the possibility of other etiological involvement in the herd. The clinical
diagnosis of LSD concurs with other cited works in which making a field level
presumptive clinical diagnosis were given due priority at the initial stages
in the emergence of an outbreak. A confirmatory laboratory diagnosis for this
incidence was not undertaken, as all efforts were directed for an effective
clinical management. However, both Polymerase Chain Reaction (PCR) and Fluorescent
Antibody Test (FAT) are the most widely employed and reliable tests in LSD diagnosis
(Brenner et al., 2006; El-Kholy
et al., 2008; Razek et al., 2009).
On the first day of LSD occurrence the following control measures were adopted
such as segregation of affected animals to a separate shed, an acaricide spray
in all the corrals and glutaraldehyde spray in the farm premises to restrict
the spread of disease. Implemented ward and watch for abortion in all groups
of herd and advised cooling system operation round the clock as the disease
complicates to produce abortion by extreme pyrexia. Local farm workers were
duly instructed regarding the sanitary measures upon their entry and exit from
the farm. Though LSD causes severe lesions on teat almost similar to pseudo
cow pox but this disease is not of zoonotic importance and did not pose threat
to handlers and milkers (Venkatesan et al., 2010).
However, in the following days, the spread was unstoppable within the herd,
as every day 40-45 animals were affected. Nevertheless, vaccination was the
immediate choice in reducing the disease spread within the herd. OIE
Terrestrial Manual (2004) which refers to two live attenuated strains of
Capripox virus that have been used specifically as vaccines for the control
of LSD: A strain of sheep and goat pox virus from Kenya and a strain from South
Africa. Whole herd vaccination was performed with Kenya VacR KGSP
0/240 102.5 TCID 50 on the third day of outbreak. Davies
(1991) quoted that good protection has been obtained with 102
in the face of an epizootic, with both the Neethling and Kenya SGPV strains
but an immunizing dose of 103.5 TCID50 is desirable for field vaccination.
However a third, different Capripox virus strain vaccine (RM 65 -Romanian
strain sheep pox vaccine) was used during LSD outbreak in Egypt in 1989/1990
and Israel had utilized this strain to control LSD outbreaks both in 1989 and
2006 (Yeruham et al., 1995; Brenner
et al., 2006). Incubation period for LSD remain largely unknown for
field outbreaks or around 4-5 weeks as against the range of 6-9 days after experimental
inoculation (Kitching, 2008). Despite the vaccination,
the disease spread was continuing in the herd possibly due to reasons such as
the vector control measures did not work efficiently and a questionable effect
of vaccination to a disease exposed population. Israel in its previous outbreaks
adopted sheep pox vaccine (RM 65 strain) on Holstein cattle (Brenner
et al., 2006). However, the farm in concern had conducted vaccination
with Kenyan SGPV strain but not with RM65 strain complying national regulations.
Vaccination in the wake outbreak to control the disease spread and the expected
immunity in the vaccinated population whilst their exposure is questionable
and this decision may be debatable. However, there was no choice in the decision
about vaccination as the disease occurred for the first time to this herd. Interestingly
in Israel, cutaneous clinical manifestation appeared in 513 cows (11%) out of
4607 cows that had been vaccinated with the RM65 strain, to LSDV infection during
the outbreak in 2006-2007. It is important although the trend was higher in
beef cattle than dairy cattle. (Brenner et al., 2009)
This clearly suggest that vaccination induced clinical manifestation is possible
in the face of an epidemic, however, there are no reports in the literature
in this regard as we had vaccinated the herd with Kenyan SGPV strain. Repeat
annual vaccination with Kenya VacR had been conducted in 2010 and
2011, till date the herd remains safe.
Role of biting insects (Stomoxys calcitrans) in the Israeli LSD outbreaks
and experimental evidence of female mosquitoes of (Aedes aegypti) in
the mechanical transmission of LSDV is well documented (Yeruham
et al., 1993, 1995; Chihota
et al., 2001). The arthropod control was a serious concern throughout
this episode within the herd. Cypermethrin spray had been performed rigorously
in the corrals since the advent but no measures could tackle the continuous
cattle- insect -cattle cycle. At once even, Ivermectin administration was considered
initially in the plan as a vector control measure and the decision was dropped
fearing the consequences it has on the food chain and on the herd. Even when
contagious transmission is considered to be inefficient route of transmission
(Davies, 1991) however, communal grazing and sharing
watering points are considered as a potential risk factor for transmission of
LSD in Ethiopia as quoted by Gari et al. (2010).
However, in an intensively managed herd like the one in state, where segregation
of affected/ disease incubating population would be constrained by space limitations
there could be a certain level (often negligible) of transmission by sharing
the water trough and at the feed bunk. Although this possibility is very rare
and hypothetical as Carn and Kitching (1995) proved
that no spread of LSDV between cattle housed in contract in the absence of arthropods
even when LSDV shed in saliva, respiratory secretions and milk.
As there is no specific antiviral treatment available for LSD infected cattle.
Systemic antibiotics were suggested for skin infections, cellulitis or pneumonia
(Davies, 1991). In this episode, treatment had been
carried out with Penicillins, Non Steroidal Anti Inflammatory Drugs (NSAIDS)
and Anti histamines to combat skin lesions, lameness and pneumonia. Clinical
management and treatment of the affected cases was carried out in different
batches to facilitate the handling, administration of medications and to expect
the any untoward signs such as abortions in dry pregnant cows. Until end of
this outbreak episode, we had handled all the treatment and recovery batches
of cows by as early as 4.30-5.00 am in the morning, as handling at higher environmental
temperature could hamper their recovery. Wound dressings were carried out with
antiseptic sprays, antibiotic sprays and fly repellant ointments. Intravenous
fluid support and nursing care were given to those recovering cows. Regardless
of the effort mortality continued. Culling of the affected herd as an interim
proposal was forwarded to the managements present and future consideration.
Milk production dropped by 40% and extended up to 65% until end of the episode
caused a huge production loss. LSD causes considerable economic losses due to
emaciation, damage to hides, infertility in males and females, mastitis, loss
of milk production (Irons et al., 2005). However,
in authors opinion, calculation of loss would never be real except for
milk production and herd mortality, but not of the several opportunities that
had been lost in the breeding life cycle of a cow in an intensively managed
herd like this with multiple thousand population since advent of LSD until six
months as the disease has significant impact on herds health. Even a short
epidemic of LSD could have devastating effects on bottom line of a dairy farm
as it affects both production and reproduction. The recovering animals/early-lactation
dairy cattle could have been greatly benefitted if inclusion of calcium salts
of palm fatty acids (Salem and Bouraoui, 2008). Rumen
protected Methionine (RPM) (Ghorbani et al., 2007)
and or a herbal galactgogue (Preciado et al., 2011)
in to their diets to boost milk yield and minimize the loss. However, these
decisions are debatable in terms of economy and adaptability to this particular
LSD recovering herd.
The 1989 LSD outbreak in Israel had clearly concluded that the spread of disease
was by the biting insect population carried in air currents from Egypt but not
by livestock movement as the country imposes strict quarantine regulations.
Contrastingly, Egypt has traced back the infected cattle imported from Ethiopia
as a source of LSDV to its outbreak in 2006 (Davies, 1991;
Yeruham et al., 1995; El-Kholy
et al., 2008). However, source of vector to this catastrophic episode
to the herd was inconclusive except to trace back any evidential record of infected
livestock movement in to Oman or to monitor unauthorized routes. The present
report also appeals to the national authorities to impose further strict import
regulations of live cattle and update regulations related with livestock movement.
Most importantly, the manuscript warrants conducting epidemiological and entomological studies in detail both at a regional and at national level as LSD reappeared after two decades in the Sultanate of Oman since its first report to OIE in 1984.
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