Acta Tropica 242 (2023) 106922

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Evidence of lumpy skin disease virus infection in camels

Ram Kumar a, #, Bhagraj Godara a, #, Yogesh Chander a, #, Jai Prakash Kachhawa b,
Ramesh Kumar Dedar a, Assim Verma a, Thachamvally Riyesh a, Yash Pal a, Sanjay Barua a,
Bhupendra N. Tripathi c, *, Naveen Kumar a, *
a
National Centre for Veterinary Type Cultures, ICAR-National Research Centre on Equines, Hisar, India
b
Department of Veterinary Medicine, Rajasthan University of Veterinary and Animal Sciences, Bikaner, India
c
Animal Science Division, Indian Council of Agricultural Research, Krishi Bhawan, New Delhi, India

A R T I C L E I N F O A B S T R A C T

Keywords: Countries in the Indian subcontinent are currently facing a deadly epidemic of lumpy skin disease (LSD). LSD is
Lumpy skin disease primarily a disease of cattle. Buffaloes may sometimes develop mild illness, however, other domestic animals are
India considered resistant to LSD. We confirmed the LSDV infection in camels as evidenced by skin nodules on the body
Camel
surface of the affected camels, isolation of LSD virus (LSDV) and amplification of LSDV-specific gene segments
Kanyan type LSDV
from the skin nodules (PCR), nucleotide sequencing of the viral genome and, demonstration of anti-LSDV an­
tibodies in serum. Phylogenetic analysis based on nucleotide sequencing of ORF011, ORF012 and ORF036
revealed that the virus (LSDV/Camel/India/2022/Bikaner) is related to the historical NI-2490/Kenya/KSGP-like
field strains which are predominantly circulating in the Indian subcontinent. This is the first report wherein LSDV
has been to infect camels.

1. Introduction
Lumpy skin disease virus (LSD) belongs to the genus Capripoxvirus of
the family Poxviridae (Tulman et al., 2001; Woods, 1988). Two other
capripoxviruses, sheepox virus (SPV) and goat pox virus (GPV) which
cause similar diseases in sheep and goats respectively, are genetically
and antigenically quite similar and cannot be distinguished serologically
(Hamdi et al., 2021; Tuppurainen et al., 2017). LSD is characterised by
fever, enlargement of lymph nodes, anorexia, depression, dysgalactia,
emaciation, and development of skin nodules, eventually resulting in a
reduction in milk yield, abortion in pregnant cattle, and sterility in bulls
(Ali et al., 1990; Flannery et al., 2022; Jalali et al., 2017). The morbidity
in LSD varies between 50-100% (Molla et al., 2017). The mortality rate
is usually low (<1%) (Casal et al., 2018), however, recent outbreaks in
Western India rendered it to be very high (Kumar and Tripathi, 2022).
The World Organisation for Animal Health (WOAH) categorizes LSD
as a notifiabledisease (OIE, 2020). It has emerged as a serious hazard for
the food security of the people in the affected areas (CABI, 2019). For
many decades since its first report from Zambia in1929 (RAS, 1931), it
has been limited to African countries. Since 2012, LSD has spread from
Africa into several European countries. In Asia, LSD was first reported in
2019 in North West China, Bangladesh and India (Roche et al., 2020;
Sudhakar et al., 2020; Tran et al., 2021) and subsequently in 2020, it
spread across many countries in Asia including Bhutan, Myanmar,
Nepal, Vietnam and Sri Lanka (Kumar and Tripathi, 2022).
Ever since its introduction in India, incidences of LSD have been
primarily observed in the eastern parts of the country without any sig­
nificant mortality (Kumar et al., 2023). The current wave of LSD, which
originated in the Indian states of Gujarat and Rajasthan in June/July
2022 has proven to be highly lethal. According to the Department of
Animal Husbandry and Dairying, Government of India, LSD has affected
about 3.3 million cattle including 1,85,600 deaths till February 2023
(DAHD, 2023). During August/September 2022, when LSD outbreaks
were at their peak, the milk production decreased by more than 26%
(Shagun, 2022).
LSD is primarily a disease of cattle. Buffaloes may sometime develop
mild illness whereas other domestic animals are considered to be
resistant to LSDV (Kumar and Tripathi, 2022). Orf virus (Parapoxvirus)
and camelpox virus (Orthopoxvirus) are well known to inefect camels but
Capripoxvirus such as LSDV has never been shown to infect and produce
any disease in camels. We herein first time report the LSDV infection in
camels which is considered as an unnatural host.

* Corresponding authors:
E-mail addresses: bntripathi1@yahoo.co.in (B.N. Tripathi), Naveen.Kumar1@icar.gov.in (N. Kumar).
#
These authors contributed equally to this work.

https://doi.org/10.1016/j.actatropica.2023.106922
Received 28 February 2023; Received in revised form 29 March 2023; Accepted 7 April 2023
Available online 7 April 2023
0001-706X/© 2023 Elsevier B.V. All rights reserved.
R. Kumar et al.
Fig 1. Clinical findings. LSDV-like skin nodules on neck, shoulder, flank (a,b) and hind limbs (c) on the body surface of the camel.
2. Materials and Methods
2.1. Ethics Statement
The study involves the collection of biological samples from camels.
Skin nodules and blood samples (3 ml each) were collected from the
affected camels (n=4) as per standard practices without using anaes­
thesia. Due consent was also obtained from the farmer (animal owner)
before the collection of the samples.
2.2. Cells
Primary lamb testicle (PLT) cells (Kumar et al., 2014) and African
green monkey kidney (Vero) cells (Khandelwal et al., 2017) were
available at the National Centre for Veterinary Type Cultures (NCVTC),
Hisar (India) and grown in Dulbecco’s Modified Eagle’s Medium
(DMEM) supplemented with antibiotics and 10-15% foetal calf serum.
2.3. Virus
Vero cell adapted LSDV (LSDV/Cattle/India/2019/Ranchi/P50) was
used for the virus neutralization assay and has been previously described
by our group (Kumar et al., 2021, 2023). Orf virus (ORFV) and camelpox
virus (CMLV) which were used as positive controls and Bovine herpes­
virus 5 (BoHV5), which was used as a negative control in PCR were
available with us in the repository of animal microbes (NCVTC, Hisar,
India).
2.4. Clinical samples
Four camels were admitted to the veterinary clinics at the Rajasthan
University of Veterinary and Animal Sciences, Bikaner (28◦ 01′ 00′′ N
73◦ 18′ 43′′ E), India for treatment of various disease ailments (impac­
tion/fistula/chest abscess). Observance of nodule-like structures on the
body surface of the camels tempted us to speculate for LSD infection.
Pieces of tissues from the nodular skin lesions were collected in 3 ml
DMEM and transported on ice to the laboratory. Samples collected from
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Acta Tropica 242 (2023) 106922
each camel include tissues from at least three skin nodules. The samples
were triturated to make a ~10% suspension in DMEM followed by
filtration through the 0.45 µM syringe filter and storage at -80◦ C until
use. Serum and blood samples were also collected from all four camels.
2.5. PCR
PCR to amplify the LSDV genome (ORF36) was carried out as per the
previously described method (Kumar et al., 2021). Briefly, total DNA
was extracted from skin nodules by DNeasy Blood & Tissue Kits as per
the instructions of the manufacturer (Qiagen, Valencia, CA, USA) and
resuspended in nuclease free water. The DNA was subjected to amplify
LSDV-specific DNA segments by PCR. Primers, melting temperatures
and extension times for amplification of LSDV ORFV36 are given in
Supplementary Table 1. For PCR amplification, each reaction tube of
20 µl contained 10 µl of Q5 High-Fidelity 2 × Master Mix (New England
BioLabs Inc.), 20 pmol of forward and reverse primers, and 5 µl of DNA
(template). The thermocycler conditions were as follows: a denaturation
step of 5 min at 95◦ C followed by 35 cycles of amplification [(30 s at
95◦ C, 30 s at 52◦ C and 40 s at 72◦ C], and a final extension step at 72◦ C
for 10 min. The PCR products were separated in a 1% agarose gel.
2.6. Nucleotide sequencing
In order to further confirm the identity of the virus (LSDV/India/
2022/Camel/Bikaner), ORF011, ORF012 and ORF036 of LSDV (Camel)
encoding GPCR, Ankyrin repeat (Ank) and RNA polymerase subunit
(RP030) proteins respectively, were amplified by PCR (For primers and
Thermalcycler condition, see Supplementary Table 1) as per the
previously described method (Kumar et al., 2021). The PCR fragments
were gel purified using the QIAquick Gel Extraction Kit (Qiagen, Hilden,
Germany) and subjected to direct sequencing using both forward and
reverse PCR primers.
2.7. Virus isolation
Virus isolation was conducted in primary lamb testicle cells as
R. Kumar et al. Acta Tropica 242 (2023) 106922

Fig 2. Identification. (a) Detection of LSDV genome in skin nodules. Pieces of the skin nodules were collected in 3 ml DMEM and subjected to DNA extraction. The
LSD-specific gene ORF012 (Ank) segment was amplified by PCR. (b) Detection of anti-LSDV antibodies in serum. Serum samples were collected at 3-6 days after the
appearance of skin nodules. Samples were initially heated at 56◦ C for 30 min to inactivate the complements. Two-fold serum dilutions were mixed with 102 TCID50 of
LSDV/Ranchi/P50 and incubated for 90 min at 37◦ C. Thereafter, virus-antibody mixture was used to infect Vero cells. At 72 hpi, the cells were observed for CPE to
determine the antibody titres. (c) Virus isolation. An aliquot of the virus (800 µl filtrate) was used to infect confluent monolayer of primary lamb testicle cells for 2 h
followed by addition of fresh growth medium. The cells were observed daily for the appearance of CPE. CPE observed at the second blind passage in one of the
samples (skin nodule) derived from camel is shown (d) Growth curve. Primary lamb testicle cells, in triplicates, were infected with virus infected cell culture su­
pernatant (obtained in blind passage 2) at MOI of 0.1 for 2 h, followed by washing with phosphate buffered saline (PBS) and addition of fresh medium. The virus
released in the infected cell culture supernatant at indicated time points was quantified by determination of TCID50/ml.

described previously (Kumar et al., 2021). Briefly, an aliquot of the virus
(800 µl filtrate) was used to infect a confluent monolayer of primary
lamb testicle cells for 2 h followed by addition of fresh growth medium.
The cells were observed daily for the appearance of cytopathic effect
(CPE).
2.8. Virus neutralization assay
Virus neutralization assay was conducted as per the previously
described method (Kumar et al., 2021). To demonstrate the anti-LSDV
antibodies, serum samples were heated at 56◦ C for 30 min to inacti­
vate the complements. Vero cells were grown in 96 well tissue culture
plates at ~90 confluency. Two-fold serum dilutions (in 50 µl volume)
were made in MEM and incubated with LSDV (102 TCID50) for 90 min.
Thereafter, virus-antibody mixture was used to infect Vero cells. The
cells were observed daily for the appearance of CPE. Final reading was
recorded at 72 hpi for the determination of antibody titres.
2.9. Phylogenetic Analysis
The ORF011, ORF012 and ORF036 of LSDV (Camel) encoding GPCR,
Ank and RP030 proteins were amplified by PCR and subjected to direct
nucleotide sequencing. The sequences were edited to 1053, 468 and 558
bp fragments respectively using BioEdit version 7.0. For evolutionary
analysis, corresponding sequences of other LSDV strains, SPV strains and
GPV strains were retrieved from the GenBank and a concatemeric
phylogenetic tree was constructed. The evolutionary history was infer­
red using the Neighbor-Joining method. The percentage of replicate
trees in which the associated taxa clustered together in the bootstrap test
(1000 replicates) is shown next to the branches. The tree is drawn to
scale, with branch lengths (above the branches) in the same units as
those of the evolutionary distances used to infer the phylogenetic tree.
The evolutionary distances were computed using the Maximum Com­
posite Likelihood method. All the ambiguous positions were removed for
each sequence pair (pairwise deletion option). Evolutionary analyses
were conducted in MEGA11.
3. Results and Discussion
LSD is primarily a disease of cattle. Buffaloes are relatively resistant
to LSD, however, a mild illness can occasionally be observed. Other
domestic animals such as sheep, goats and camels are considered to be
resistant to LSDV infection (Sprygin et al., 2019). There was a history of
extensive LSD outbreaks in the surrounding area when camels were
admitted to the university veterinary clinics in Bikaner. Besides, camels
also had a history of close contact with LSD infected cattle. Skin nodules,
ranging in size from 4-8 mm in diameter were observed on the neck,
shoulder, flank (Fig. 1a,b) and hind legs (Fig. 1c) in camels. However,
the size of the skin nodules in camels was quite smaller than usually seen
in LSD affected cattle (10-50 mm) (Kumar et al., 2021).
These skin nodules were self-limiting (within 3-4 days) and none of
these skin nodules developed into pustules/scab/sit fast, as observed in
cattle (Kumar et al., 2021). The history of camels in close contact with
the LSD-infected cattle and skin nodules on the body surface was pri­
marily suggestive of LSDV infection. The tissues collected from the skin
nodules were processed to carry out various virological assays, per the

3
R. Kumar et al.
standard procedures (Kumar et al., 2021). In PCR, the skin nodules from
camels were found positive for Capripoxvirus (LSDV)-specific DNA
segment (RPO30) (Fig. 2a) but twere negative for Parapoxvirus- and
Orthopoxvirus-specific gene segments (Supplementary Table 2 and Sup­
plementary Fig 1). This further confirmed the LSDV infection in camels.
Three of the four camels also showed the presence of anti-LSDV
antibodies (titer ranging from 8-16) in the virus neutralization assay
(Fig 2b). In LSDV, the detectable amount of antibodies is usually
observed at ~14 days following LSDV infection, whereas peak levels are
detected at about a month following infection (Moller et al., 2019;
Neamat-Allah, 2015; Wolff et al., 2021). We collected serum samples 3-6
days after the appearance of the skin nodules. One animal had no
detectable antibody titer which is presumably due to the early collection
of serum samples.
For virus isolation, the virus recovered from the skin nodules was
used to infect the primary lamb testicle cells. Infection of the clinical
samples did not reveal any cytopathic effect (CPE) up to 7 days post-
infection in any of the four samples subjected to virus isolation. There­
after, the infected cells were freeze-thawed twice and the resulting su­
pernatant (called the first blind passage) was used to infect fresh cells.
CPE was observed in one (A15/12) out of the four samples on the second
blind passage (day 3 post-infection) (Fig 2c). The virus collected at day 4
post-infection in the second blind passage was quantified by determi­
nation of TCID50/ml.
Further, the growth curve of the virus was evaluated in primary lamb
testicle cells. There was a progressive increase in the number of virus
particles released in the infected cell culture supernatant from 12 hour
post-infection (hpi) to 72 hpi, before becoming stable at 96 hpi (Fig 2d).
This was clearly indicative of the generation of new progeny virus
particles and hence suggestive of the adaptation of the virus in the cell
culture system. A few virus particles detected at ≤12 hpi were pre­
sumably indicative of the virus input (used to infect cells). The virus was
further bulk cultured and deposited in the National repository (NCVTC,
Hisar, India) with an Accession Number of VTCCAVA371.
In order to compare and determine the phylogenetic relationship of
the virus under study (LSDV/Camel/India/2022/Bikaner) with other
4
Acta Tropica 242 (2023) 106922
Fig 3. Phylogenetic analysis. ORF011,
ORF012 and ORF036 of LSDV (Camel) encod­
ing GPCR, Ank and RP030 proteins were
amplified by PCR and subjected to direct
nucleotide sequencing as descried previously.
The sequences were edited to 1053, 468 and
558 bp fragments respectively, using BioEdit
version 7.0. For evolutionary analysis, corre­
sponding sequences of other LSDV strains, SPV
strains and GPV strains (both field and vaccine
strains) were retrieved from GenBank and a
concatemer-based phylogenetic tree was
constructed.
LSDV, sheepox virus (SPV) and goatpox virus (GTPV) strains, ORF011,
ORF012 and ORF036 encoding GPCR, Ank and RP030 proteins were
amplified by PCR (Supplementary Table 1) and subjected to direct
sequencing using forward and reverse PCR primers. The nucleotide se­
quences of ORF011, ORF012 and ORF036 were deposited in the Gen­
Bank with Accession Numbers of OP473922, OP473920 and OP473924,
respectively. The sequences were edited to 1053, 468 and 558 bps
fragments respectively using BioEdit version 7.0. These sequences,
together with the corresponding nucleotide sequences from other LSDV/
SPV/GPV strains (including both vaccine and field strains) retrieved
from the GenBank, were used to compare for homology (Supplementary
Table 3), besides preparing a consensus linear phylogenetic tree (Fig 3).
The limited nucleotide sequence analysis revealed that LSDV/Camel/
India/2022/Bikaner is identical to the cattle LSDV strain- the NI-2490/
Kenya/KSGP-like field LSDV strain which is predominantly circulating
in the Indian subcontinent. However, to precisely dissect the camel-
specific genetic signatures (if any) in the viral genome, whole genome
sequence data of large numbers of camel and cattle LSDV isolates needs
to be generated. This needs further investigation.
Poxviruses are a large family of DNA viruses capable of infecting and
causing disease in a wide variety of animals including humans. While
smallpox has been eradicated, the monkeypox virus has become an in­
ternational concern for human health. Like monkeypox in humans,
LSDV has emerged as the most important pathogen with regards to an­
imal health (Byadovskaya et al., 2022; Krotova et al., 2022). The pox­
viruses are considered host specific (Haller et al., 2014b). However, for
reasons unknown, they may sometimes break the host tropism to infect
unnatural hosts. In this regard, zoonotic infections of CMLV (Bera et al.,
2011), buffalopox virus (Bhanuprakash et al., 2010; Marinaik et al.,
2018) and monkeypox virus (Alakunle and Okeke, 2022; Hutson et al.,
2007; Parker et al., 2007) have evoked special concerns in infection
medicine.
The prototype poxvirus vaccinia, is able to bind and enter every cell
type tested. Till date, no receptor has been unequivocally identified for
any poxvirus (Haller et al., 2014a). The high density of infection in the
endemic areas, close contact with the cattle (highly susceptible to LSDV)
R. Kumar et al.
population and increased vector population in the rainy season in India
seem to have contributed to the adaptation of LSDV in camels. However,
the precise viral and host factors that allowed the adaptation of LSDV to
camels remain unknown. Identification of the viral and host factors
responsible for adaptation of the LSDV in camels, along with the iden­
tification of putative host cell receptors is essential and needs further
investigation.
4. Conclusion
The history of the camels in close contact with LSDV infected cattle,
the development of skin nodules on the body surface, demonstration of
virus and viral genome in the skin nodules and most importantly, the
detection of anti-LSDV antibodies in the serum is strongly suggestive of a
productive LSDV infection in camels. This necessitates the inclusion of
camels in the epidemiology and control of LSDV infection in cattle.
CRediT authorship contribution statement
Naveen Kumar: Conceptualization, data curation, investigation and
writing-original draft. Ram Kumar, Bhagraj Godara, Yogesh Chander
and Assim Verma: Data curation, methodology and investigation. Jai
Prakash Kachhawa, Ramesh Kumar Dedar, Thachamvally Riyesh,
Yash Pal, Sanjay Barua and Bhupendra N. Tripathi: Data curation
and review and editing. All authors read and approved the final
manuscript.
Supplementary material
Supplementary data associated with this article can be found, in the
online version.
Declaration of Competing Interest
None of the authors of this paper have any financial or personal
relationship with people or organisations that could inappropriately
influence or bias the content of the paper.
Data availability
No data was used for the research described in the article.
Acknowledgements
This work was supported by Indian Council of Agricultural Research,
Grant Number IXX11882 and IXX16675.
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.actatropica.2023.106922.
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