LSD symposium - E. Klemen - Modes of transmission of lumpy skin disease

1. Modes of transmission of
Lumpy Skin Disease
Eyal Klement
Koret School of Veterinary Medicine, the Hebrew University, Jerusalem, Israel

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Different modes of transmission
• Direct vs. indirect
• Vertical vs. horizontal
• Clinically vs. sub-clinically
• Short distance vs. long distance
Lumpy Skin Disease symposium, Rome, March 2023

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Direct vs. indirect
• Direct transmission:
Direct transmission occurs when a susceptible host contracts an
infection, either by physical contact with an infected host or by
contact with the latter's infected discharges (Thrusfield, 2005).
• Indirect transmission:
involves an intermediate vehicle, living or inanimate, that transmits
infection between infected and susceptible hosts (Thrusfield, 2005).
Lumpy Skin Disease symposium, Rome, March 2023

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Direct vs. indirect: Which is more important?
• Indirect transmission of LSD is probably far more important than
direct transmission!
• Supporting evidence:
• No transmission of the virus between clinically infected cattle to susceptible
cattle housed together, in a no-vector environment (Carn and Kitching, 1995).
• Mathematical modelling of an outbreak in Israel showed that indirect
transmission could explain the entire outbreak dynamics (Magori-Cohen et al. 2012).
• Seasonality
• Spread pattern
Lumpy Skin Disease symposium, Rome, March 2023

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No transmission of the virus between clinically infected cattle to
susceptible cattle housed together, in a no-vector environment (Carn and
Kitching, 1995).
28 days
28 days
LSDV
Lumpy Skin Disease symposium, Rome, March 2023

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non-vector-borne transmission of lumpy skin
disease virus (Kononov et al. 2020)
• The recombinant (‘Saratov’) LSD virus
• Bulls inoculated and placed one near each other along a trough with
limited mobility.
33 days
Lumpy Skin Disease symposium, Rome, March 2023

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What are the potential routes of virus spread and which is
more important?
Mathematical modelling of LSD transmission in an
outbreak (Magori-Cohen et al. 2012).
Lumpy Skin Disease symposium, Rome, March 2023

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Lumpy Skin Disease symposium, Rome, March 2023

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α,β,γ,δ
Lumpy Skin Disease symposium, Rome, March 2023

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Results and conclusion
>>
Indirect transmission (probably by blood
sucking flying insects) is the most
important route of virus transmission
Lumpy Skin Disease symposium, Rome, March 2023

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Routes of indirect transmission
• Arthropod vectors
• Iatrogenic (via needles)
• Drinking from the same water trough
or via feed.
Lumpy Skin Disease symposium, Rome, March 2023

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Vertical transmission?
• There is no clear evidence for transmission of virus from mother to fetus.
• Transmission via milk was suggested though it was not proved in insect
proof settings .
• Transmission via semen:
• Virus was found in semen, 8 to 159 days PI (Irons et al. , 2005).
• Insemination of naïve heifers with bull’s semen spiked with high loads of virus
resulted in infection and sometime severe disease. All heifers aborted shortly after
insemination (Annandale et al., 2014).
• However, the virus concentration due to natural infection is much lower (Babiuk et al,
2008).
• Effective vaccination prevents virus excretion in semen (Osuagwuh et al. 2007).
Lumpy Skin Disease symposium, Rome, March 2023

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Are subclinical animals infective?
• Up to 50% of infected animals might not show clinical signs, though they
may be viremic and sero-convert (Tuppurainen et al, 2005).
• LSDV was transmitted by ticks fed on healthy looking skin (Tuppurainen et al, 2013).
• Stomoxys calcitrans transmitted virus from sub-clinically infected animals
to contacts (Soheir et al. 2019)
• However, there is much evidence to show that if such transmission does
exist, it is minor and probably negligible relative to transmission by sick
animals:
• Viral load in intact skin is much lower than in lesions (Babiuk et al., 2008).
• Viral load in blood is intermittent and much lower than in lesions (Babiuk et al., 2008).
• LSD outbreaks in Israel were controlled using only modified stamping out and a
vaccine with very low effectiveness.
Lumpy Skin Disease symposium, Rome, March 2023

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Spread of lumpy skin disease
• The average spread recorded
in the Balkans was 7.3
Km/week (Mercier et al. 2017).
• However, spread distribution
was highly skewed with
maximal distance of 543.6
Km/week
(Mercier et al. 2017).
Lumpy Skin Disease symposium, Rome, March 2023

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Pattern of spread of lumpy
skin disease in the Balkans
(Mercier et al. 2017).
Do you note any particular
pattern?
Lumpy Skin Disease symposium, Rome, March 2023

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Spread mechanism
• Short distance:
• Movement of infected animals.
• By actively flying vectors.
• Long distance:
• Movement of infected animals
• Vectors carried by winds (Klausner et al. 2017)?
Lumpy Skin Disease symposium, Rome, March 2023

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Synoptic systems associated with winds into Israel (Klausner
et al. 2017)
Lumpy Skin Disease symposium, Rome, March 2023

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Events of winds from infected locations in Egypt to Peduyim in Israel,
1989, up to 90 days before outbreak occurrence (Klausner et al. 2017)
Lumpy Skin Disease symposium, Rome, March 2023

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Conclusions
• LSDV can be transmitted both by direct and indirect contact.
• The epidemiological role of indirect transmission (i.e. by vectors is
probably much more important)
• It is unknown if the new recombinant ‘Saratov’ virus is more
susceptible for direct transmission
• Vertical transmission probably does not occur in natural settings
though in experimental setting it does occur
• Spread velocity is usually about 10 Km a week.
• However long distance spread can occur, mostly by animal movement
and maybe by winds (though probably this is minor).
Lumpy Skin Disease symposium, Rome, March 2023

20. Protecting people, animals, and the environment every day
Drawings: FAO/Chiara Caproni
Thanks!

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References:
• Thrusfield M. Veterinary epidemiology 3rd edition, 2005.
• Carn, V.M., Kitching, R.P., 1995. An investigation of possible routes of transmission of lumpy skin disease virus (Neethling). Epidemiol Infect 114, 219-
226.
• Aleksandr, K., Olga, B., David, W.B. et al. 2020. Non-vector-borne transmission of lumpy skin disease virus. Sci Rep 10, 7436.
• Magori-Cohen, R., Louzoun, Y., Herziger, Y., Oron, E., Arazi, A., Tuppurainen, E., Shpigel, N.Y., Klement, E., 2012. Mathematical modelling and evaluation
of the different routes of transmission of lumpy skin disease virus. Veterinary research 43, 1.
• Irons, P.C., Tuppurainen, E.S., Venter, E.H., 2005. Excretion of lumpy skin disease virus in bull semen. Theriogenology 63, 1290-1297.
• Annandale, C.H., Holm, D.E., Ebersohn, K., Venter, E.H., 2014. Seminal transmission of lumpy skin disease virus in heifers. Transbound Emerg Dis 61,
443-448.
• Babiuk, S., Bowden, T.R., Parkyn, G., Dalman, B., Manning, L., Neufeld, J., Embury-Hyatt, C., Copps, J., Boyle, D.B., 2008. Quantification of lumpy skin
disease virus following experimental infection in cattle. Transbound Emerg Dis 55, 299-307.
• Osuagwuh, U.I., Bagla, V., Venter, E.H., Annandale, C.H., Irons, P.C., 2007. Absence of lumpy skin disease virus in semen of vaccinated bulls following
vaccination and subsequent experimental infection. Vaccine 25, 2238-2243.
• Tuppurainen, E.S., Venter, E.H., Coetzer, J.A., 2005. The detection of lumpy skin disease virus in samples of experimentally infected cattle using
different diagnostic techniques. Onderstepoort J Vet Res 72, 153-164.
• Tuppurainen, E.S., Lubinga, J.C., Stoltsz, W.H., Troskie, M., Carpenter, S.T., Coetzer, J.A., Venter, E.H., Oura, C.A., 2013. Mechanical transmission of
lumpy skin disease virus by Rhipicephalus appendiculatus male ticks. Epidemiol Infect 141, 425-430.
• Mercier, A., Arsevska, E., Bournez, L., Bronner, A., Calavas, D., Cauchard, J., Falala, S., Caufour, P., Tisseuil, C., Lefrancois, T., Lancelot, R., 2017. Spread
rate of lumpy skin disease in the Balkans, 2015-2016. Transbound Emerg Dis.
• Klausner, Z., Fattal, E., Klement, E., 2015. Using synoptic systems' typical wind trajectories for the analysis of potential atmospheric long distance
dispersal of lumpy skin disease virus. Transbound Emerg Dis.
• Shumilova I, Nesterov A, Byadovskaya O, Prutnikov P, Wallace DB, Mokeeva M, Pronin V, Kononov A, Chvala I, Sprygin A. A Recombinant Vaccine-like
Strain of Lumpy Skin Disease Virus Causes Low-Level Infection of Cattle through Virus-Inoculated Feed. Pathogens. 2022 Aug 16;11(8):920.