Mathematical modelling and evaluation of the different routes of transmission of lumpy skin disease virus

Abstract

Lumpy skin disease (LSD) is a severe viral disease of cattle. Circumstantial evidence suggests that the virus is transmitted mechanically by blood-feeding arthropods. We compared the importance of transmission via direct and indirect contact in field conditions by using mathematical tools. We analyzed a dataset collected during the LSD outbreak in 2006 in a large dairy herd, which included ten separated cattle groups. Outbreak dynamics and risk factors for LSD were assessed by a transmission model. Transmission by three contact modes was modelled; indirect contact between the groups within a herd, direct contact or contact via common drinking water within the groups and transmission by contact during milking procedure. Indirect transmission was the only parameter that could solely explain the entire outbreak dynamics and was estimated to have an overall effect that was over 5 times larger than all other possible routes of transmission, combined. The R0 value induced by indirect transmission per the presence of an infectious cow for 1 day in the herd was 15.7, while the R0 induced by direct transmission was 0.36. Sensitivity analysis showed that this result is robust to a wide range of assumptions regarding mean and standard deviation of incubation period and regarding the existence of sub-clinically infected cattle. These results indicate that LSD virus spread within the affected herd could hardly be attributed to direct contact between cattle or contact through the milking procedure. It is therefore concluded that transmission mostly occurs by indirect contact, probably by flying, blood-sucking insects. This has important implications for control of LSD.

Figure 1

Location of the groups in the affected herd. A. Milking pallor B. Euthanasia area. 1. First lactation cows 2. Second lactation cows. 3. Pre-calving group 4. Replacement heifers pending insemination and in early pregnancy 5. Replacement heifers (10-12 months old) 6. Pregnant replacement heifers 7. Dry cows. 8. High parity 9. Fattening calves. 10. Suckling calves.

Figure 2

Epidemic curve of generalized LSD during the outbreak in Ein-Zurim, 2006. Black columns represent cases for which the date of disease appearance is definite. Grey columns represent cases for which date of disease appearance is not definite. The dashed lines represent their earliest assumed date of appearance. Double headed arrows represent the time period during which these cases may have first appeared. Black arrow represents vaccination date.

Figure 3

Clinical appearance of lumpy skin disease during the outbreak in Ein-Zurim in 2006. A. Localized lumpy skin disease. B. Generalized disease C. Generalized disease with limb oedema.

Figure 4

Spread of generalized LSD between cattle groups. See Table 2I for group description. Grey scale indicates daily incidence in each group.

Figure 5

Fit of transmission model with actual data of LSD outbreak in Ein-Zurim during 2006. Bars - actual data. Each line represents a model. Note that the parameters of each model were optimized independently. A. Epidemic curve. B. Average daily incidence in each group during the outbreak period.

Figure 6

Sensitivity analysis of alpha (indirect contact) and beta (direct contact). Surface color represents maximum likelihood for the model fit with the real data of LSD outbreak in Ein-Zurim, 2006. Note, that the model is significantly more sensitive to alpha than to beta, primarily around the optimal value.

Figure 7

Ratio between direct (beta + gamma) and indirect (alpha) transmission rates as a function of: A. Fixed average and standard deviation of the incubation time. B. Ratio of susceptible cattle out of cattle that did not show clinical signs.