The potential spread of severe footrot in Norway if no elimination programme had been initiated: a simulation model
- Gry M Grøneng^{1}Email author,
- Synnøve Vatn^{2},
- Anja Bråthen Kristoffersen^{1},
- Ola Nafstad^{2} and
- Petter Hopp^{1}
https://doi.org/10.1186/s13567-015-0150-y
© Grøneng et al.; licensee BioMed Central. 2015
Received: 24 July 2014
Accepted: 14 January 2015
Published: 20 February 2015
Abstract
When severe footrot was detected in Norway in 2008, a surveillance programme was initiated and followed by an elimination programme. By 2013 the disease had spread to two of 19 counties and a total of 119 (1%) sheep flocks had been diagnosed with severe footrot. A simulation model was developed to estimate the potential spread of severe footrot in Norway and to estimate the relative importance of the different spreading routes. The model parameters were based on the rate of spread of the first 38 diagnosed cases and the management and climatic factors particular for Norway. The model showed that by 2013, severe footrot would have spread to six counties and infected 16% of the sheep flocks if no elimination programme had been initiated. If this is compared with the 1% of flocks that were diagnosed in Norway by 2013, there seems to be a large effect of the implemented footrot elimination programme. By 2035, it was estimated that severe footrot would have spread to 16 counties and 64% of the sheep flocks. Such an extensive spread would probably impose a large negative impact on the sheep industry and welfare of the sheep. The most effective way to curb the spread of severe footrot was by decreasing the within county infection rate. This could be achieved by decreasing the contact between flocks or by decreasing the environmental load of D. nodosus, for example by footbathing sheep, culling diseased sheep or eliminating severe footrot in the flock.
Introduction
Footrot is well known in sheep-producing countries worldwide. The clinical signs range from mild inflammation of the interdigital skin to under-running and separation of the hoof horn from the sensitive tissues [1]. Footrot is a painful disease and causes lameness, poor welfare and affects ewe and lamb productivity [2,3]. Dichelobacter nodosus (D. nodosus), a Gram negative anaerobic bacterium, is the causative agent of footrot in small ruminants [1]. D. nodosus is divided into benign and virulent strains that can be differentiated in the laboratory by a gelatin gel test [4]. Clinical signs are often more severe when sheep are infected with the virulent D. nodosus strain than with the benign strain.
Data used for estimating minimum, mode and maximum infection rate of severe footrot in Rogaland
Rogaland excluding Rennesøy (minimum) | Whole of Rogaland (mode) | Rennesøy (maximum) | ||||
---|---|---|---|---|---|---|
Number of sheep flocks | 2490 | 2597 | 107 | |||
Year | Assumed infected | Predicted infected | Assumed infected | Predicted infected | Assumed infected | Predicted infected |
2005 | 1 | 1 | 1 | 1 | 0 | 0 |
2006 | ND | 3 | ND | 3 | 1 | 1 |
2007 | ND | 9 | ND | 14 | ND | 4 |
2008 | 26 | 26 | 38 | 48 | 12 | 13 |
Regional percentage of infected flocks in 2008 | 1.0% | 1.5% | 11.2% | |||
Estimated infection rate (β) | 1.13 | 1.31 | 1.36 |
The aim of this study was to estimate the potential spread of severe footrot in Norway if no elimination programme was implemented and estimate the importance of the different spreading routes of virulent D. nodosus. The developed model was based on the infection rate of the first diagnosed cases and the management and climatic factors specific to Norway.
Material and methods
A stochastic compartmental model can be used to simulate spread of disease within a population [11]. In a SILI-compartmental model, the susceptible(S), infected(I) and low susceptible(L) compartments and the transmission of flocks between these compartments describe the infection dynamics of the population. The susceptible flocks are not, and have not been, infected with the agent causing the disease. The infected flocks have at least one sheep infected with the agent causing disease and could infect susceptible or low susceptible flocks. The low susceptible flocks do not have any animals carrying the infection, and have a smaller contact network than the susceptible flocks, hence are less at risk of acquiring a disease than the susceptible flocks. The low susceptible flocks comprise of flocks with natural barriers towards other sheep flocks (called isolated flocks) and flocks that have recovered from the disease and by this increased their biosecurity measures (called recovered flocks). The latent period is assumed to be zero, and the immunity period for a flock is negligible.
In the model, flocks are transferred from one compartment to another at different rates. The infection rate (β) is the rate at which susceptible flocks become infected. This is dependent on the number of contacts, and the risk of transmission of disease per contact. The recovery rate (σ) is the rate of recovery of infected flocks, and which are accordingly assigned to the low susceptible compartment. The reversion rate (Ɣ) is the rate at which low susceptible flocks become infected, and by this transferred to the infected compartment.
Spread within subpopulations
Subpopulations can be defined if the spread of disease is not uniform in the population [12], but highly reduced from one geographical area to another. Each subpopulation is then modelled with their own SILI-compartmental model with their own infection, recovery and reversion rate. These rates are based on specific values for each subpopulation that influence the spread of the disease in question.
Spread between subpopulations
Spread of disease is expected to be faster within the subpopulations than between two subpopulations as flocks within each subpopulation are expected to have more contact than flocks from two different subpopulations. Different types of contact between flocks in separate subpopulations may occur, leading to different transmission routes. Each transmission route between subpopulations are specified and quantified separately. Only susceptible flocks in the subpopulations are expected to be infected by other subpopulations as most of the low risk flocks have increased biosecurity and thereby will not be infected through the between subpopulation transmission route.
Model
where i is the subpopulation receiving the infection, j is the subpopulation transmitting the infection and ƴ is the time interval in years, S is the number of susceptible flocks, I is the number of infected flocks, L is the number of low susceptible flocks, β is the rate at which susceptible flocks become infected, σ is the rate at which infected flocks recover and hence become low susceptible flocks, γ is the rate at which low susceptible flocks become infected, θ, δ and τ is three possible ways of introduction of infection between subpopulations.
As the starting point for the simulations, the flocks infected with the disease was assigned to the infected compartment, the isolated flocks were assigned to the low susceptible compartment, and the remaining flocks were assigned to the susceptible compartment. Year was the time step and the model was run for the number of years desired.
Adaptation of the model to footrot in Norwegian sheep flocks
A SILI-compartmental model was developed for estimating the spread of severe footrot in Norwegian sheep flocks without an elimination program. The isolated flocks in the low susceptible compartment were defined as sheep farms more than 3 km away from any other sheep farm. This was based on a study by Grøneng et al. [13] which showed that a geographic distance of more than 3 km between the main buildings of different sheep farms was not a significant risk factor in the univariable analysis. We interpret this as sheep farms with more than 3 km distance to the nearest sheep farm have a lower risk of contracting footrot.
The infection rate of footrot was calculated based on the rate of spread from the introduction of footrot in Norway in 2005 until the initiation of the elimination programme in 2009. At this time, severe footrot had only been detected in the county of Rogaland, but since different regions within the county possessed highly different rate of spread, the infection rate was expressed by a Pert distribution. Rogaland County excluding Rennesøy, Rogaland County with Rennesøy and the municipality of Rennesøy was the regions used to calculate the minimum (min), mode (mod) and maximum (max) infection rate respectively. The rates were then used in the Pert distribution.
To estimate the infection rate of the regions, the total number of sheep flocks and the number of flocks assumed to be infected with severe footrot in the region, from the introduction of the disease (2005 in Rogaland and 2006 in Rennesøy) until the initiation of the elimination programme in 2009 was used (Table 1). The infection rate was simulated based on Equations 1–3, with a constant annual recovery rate (σ) of 5.3% and a reversion rate (Ɣ) of 1/3 of the infection rate (see below for descriptions of recovery and reversion rate). The assumed number of infected flocks was the number detected in the footrot outbreak in Norway, and the predicted median number of infected flocks was as close to this number as possible. The appurtenant infection rate was used in the model. The min, mod and max predicted median number of infected flocks and the appurtenant infection rates in parentheses were 26 (1.13), 48 (1.31) and 13 (1.36), respectively (Table 1). The Pert distribution for the infection rate for Rogaland was then (β_{Rog} ~ Pert (1.13, 1.31, 1.36)).
The recovery rate was based on spread of severe footrot without an elimination programme and hence no compensation for sanitation or other measures to eliminate the disease. The recovered flocks have therefore either undergone sanitation procedure at their own cost or recovered from the disease spontaneously. Two of 38 flocks completed a successful sanitation procedure at the farmers own expense in 2008 (Vatn S, Healthy Feet project, personal communication), corresponding to a recovery rate of 5.3% per year. Some of the flocks might also recover from the disease with no intervention. Since it takes a long time for sheep in a flock to recover without human intervention [14], the percentage of these flocks is thought to be small and was not included. The recovery rate was assumed to be constant for all years.
Since none of the flocks which completed a successful sanitation procedure at the farmers own expense in 2008 was re-infected, the reversion rate could not be calculated based on data. The reversion rate was therefore sat based on knowledge of the infection dynamics. The susceptible flocks were assumed to have a three times higher infection rate than the low susceptible flocks, hence a reversion rate of (Ɣ = β/3) was used.
Spread within subpopulations in Norway
Overview of demographic data, climatic rate and infection rate for modelling spread of severe footrot
County | N ^{ o } of sheep flocks (nSh) | N ^{ o } of cattle herds (nCa) | N ^{ o } of combined flocks ( nShCa) | N ^{ o } of isolated flocks | Mean number of neighbouring flocks ( \( {\overline{n}}_{1\boldsymbol{km},\boldsymbol{i}} \) ) | Climatic rate (Cl _{ i } /Cl _{ Rog } ) | Infection rate (β) (minimum, mode, maximum) |
---|---|---|---|---|---|---|---|
Østfold | 160 | 360 | 43 | 49 | 0.2 | 0.61 | 0.04, 0.05, 0.05 |
Akershus | 226 | 359 | 45 | 43 | 0.8 | 0.61 | 0.17, 0.19, 0.20 |
Oslo | 8 | 5 | 4 | 6 | 0.0001* | 0.67 | 0.01, 0.01, 0.01 |
Hedmark | 669 | 1108 | 200 | 99 | 1.4 | 0.51 | 0.24, 0.28, 0.29 |
Oppland | 1323 | 2224 | 324 | 60 | 1.6 | 0.51 | 0.28, 0.32, 0.34 |
Buskerud | 552 | 593 | 111 | 53 | 1.5 | 0.56 | 0.29, 0.33, 0.35 |
Vestfold | 129 | 225 | 29 | 25 | 0.3 | 0.69 | 0.07, 0.08, 0.09 |
Telemark | 372 | 360 | 72 | 54 | 1.3 | 0.67 | 0.30, 0.35, 0.36 |
Aust-Agder | 220 | 250 | 47 | 60 | 0.8 | 0.76 | 0.21, 0.24, 0.25 |
Vest-Agder | 450 | 583 | 150 | 45 | 1.2 | 0.93 | 0.38, 0.44, 0.46 |
Rogaland | 2597 | 2735 | 1297 | 20 | 3.3 | 1 | 1.13, 1.31, 1.36 |
Hordaland | 1997 | 1457 | 603 | 37 | 2.3 | 1 | 0.79, 0.91, 0.95 |
Sogn og Fjordane | 1617 | 1756 | 625 | 59 | 2.5 | 0.97 | 0.83, 0.96, 1.00 |
Møre og Romsdal | 1053 | 1880 | 358 | 94 | 1.2 | 0.89 | 0.37, 0.42, 0.44 |
Sør-Trøndelag | 728 | 1729 | 187 | 99 | 1.1 | 0.62 | 0.23, 0.27, 0.28 |
Nord-Trøndelag | 524 | 1737 | 178 | 98 | 0.6 | 0.67 | 0.14, 0.16, 0.17 |
Nordland | 1045 | 1366 | 272 | 169 | 0.8 | 0.73 | 0.20, 0.23, 0.24 |
Troms | 522 | 442 | 92 | 92 | 0.8 | 0.5 | 0.14, 0.16, 0.16 |
Finnmark | 123 | 192 | 26 | 42 | 0.5 | 0.38 | 0.07, 0.08, 0.08 |
The infection rate calculated earlier was only based on the rate of spread within the county of Rogaland. To calculate the rate of spread within each of the other counties, values which would interfere with the spread of footrot are quantified and used to adjust the minimum, mode and maximum within county infection rate for Rogaland.
The fraction between the climatic factors in county i and the climatic factor in Rogaland was incorporated in Equation 5 to adjust the infection rate within each county.
Another value expected to interfere with the infection rate of footrot was the density of sheep farms within each county. Grøneng et al. [13] showed that a risk factor for contracting the disease is a sheep farm located less than 1 km from a sheep farm positive for severe footrot. The distances between farms were calculated based on the locations of the main building on each farm. Hence, for each sheep farm, the number of other sheep farms within 1 km (neighbour farms) was obtained. Based on this, the mean number of neighbour farms to the sheep farms within each county (\( {\overline{n}}_{1 km,i} \)) was calculated (Table 2). The fraction between the mean number of sheep farms within 1 km in county i and the county Rogaland was used to adjust the infection rate in county i (Equation 5). By using the knowledge of the spread of disease in the county of Aust-Agder, the effect of the fraction between counties was adjusted. In 2013, 14 flocks in the county of Aust-Agder were diagnosed with severe footrot, and epidemiological investigations indicate that sheep moved from the county of Rogaland in 2006 were the source. The spread from the introduction in 2006 to 2013 was simulated based on Equations 1–3, and a value k, adjusting the effect of the density factor between Aust-Agder and Rogaland, was chosen so that the median value of 2000 replicates matched the number of infected flocks in Aust-Agder in 2013. A median of 14 (range 1–26) infected flocks was predicted for k = 2.3 (Equation 5).
where i is the county, and Rog is Rogaland County.
The recovery rate was not expected to differ between counties and was expected to be constant for every year. The reversion rate for each county was defined as one third of the infection rate (Ɣ_{ i } = β_{i}/3).
Spread between subpopulations in Norway
The spread of footrot between counties in Norway was modelled taking three potential transmission routes into consideration: 1) movement of sheep between counties, 2) movement of cattle between counties, and 3) introduction by sharing of common pastures (Figure 1).
Introduction from other counties through sheep movement (θ)
Although there is a general ban on movement of sheep from one county to another because of maedi and scrapie, derogations from the legislation can be authorised by the Norwegian Food Safety Authority. Two movements of sheep between counties were recorded in 2013 (MATS, the supervision system of the Norwegian Food Safety Authority). There may have been movements of sheep that have not been reported to the central Food Safety Authority, but these are believed to be minimal. We therefore assumed that some of the sheep in 0.05% of the flocks in a county would be moved to each of the neighbouring counties each year. In addition, some of the sheep in 0.025% of the flocks in a county would move sheep to each of the counties bordering on neighbouring counties each year. Thus the number of movements from county j to county i was estimated (MSh _{ j,i }), and used to calculate the introduction of severe footrot to other counties (Equation 7). For Norway as a whole, this is equivalent to approximately 44 between county movements of sheep each year. As this is more than reported to the Norwegian Food Safety Authority, we believe the effect of moving sheep across county borders has been overestimated rather than underestimated.
The number of sheep moved was based on the knowledge that mostly rams are purchased, and since the sheep flocks are small, rarely more than two rams are acquired at the same time. The lowest prevalence was based on one infected sheep in a flock of 100 sheep. The highest prevalence was based on PCR examination of all sheep in three flocks infected with severe footrot, and the median of these values was used. This was chosen since only sheep from flocks with a veterinary health certificate may be moved across county borders. We therefore believe that flocks with a prevalence above 0.65 would not be allowed to move sheep because they would show pronounced clinical signs of footrot.
where i is the county receiving infectn, and j is the county transmitting the infection, I is the number of infected sheep flocks, nSh is the total number of sheep flocks, MSh is the number of flocks that have moved sheep, and S is the number of susceptible sheep flocks.
Introduction from other counties through cattle movement (τ)
where i is the county receiving infection, and j is the county transmitting the infection.
Introduction from other counties through sharing of common pasture ( \( \delta \))
where N _{ f } is the number of sheep flocks on pasture, A _{ past } is the geographic area of the pasture in km^{2} and n is the number of pastures.
The climate of the common pastures (Cl _{ past }) could not be calculated in the same way as the within county climate because we did not have specific geographical points, but rather large areas across which the sheep flocks were spread. The common pastures are often situated at a higher altitude than the general location of sheep farms, and the climate is often colder and dryer. Given this knowledge, we believe that the climate on common pasture has a lower value than the climate in any of the counties, so the climatic rate of common pasture (Cl _{ past } /Cl _{ Rog }) was assumed to be 0.3, lower than the lowest climate rate (Table 2). The climatic rate was constant for all years, and was used in the calculation of the common pasture infection rates as shown in Equation 10.
where i is the county receiving infection, and j is the county transmitting the infection.
Model for Norway
As the starting point for the simulations, one flock in the county of Rogaland was assigned to the infected compartment, the isolated flocks in each county were assigned to the low susceptible compartment in the respective counties, and the remaining flocks in each county were assigned to the susceptible compartments. When the probability of transferring flocks between compartments resulted in decimal number of flocks, the decimal number was converted to an integer by performing a Bernoulli trial with the decimal fraction as the probability. The county results were aggregated to give the results for Norway.
Scenarios
Basic scenario
The basic scenario was simulation of the spread of severe footrot without any elimination or control with input values as presented in Tables 1 and 2. For all the scenarios where input parameters were changed, the basic scenario was used as the reference.
Scenarios with different control measures
The disease can be controlled by reducing the within county or between county transmissions compared to the basic scenario. Scenarios with a 20%, 40%, 60% and 80% lower infection rate within the counties were modelled. Scenarios with 20%, 40%, 60%, 80% and 100% less movement of sheep between counties were modelled. Scenarios with 20%, 40%, 60%, 80% and 100% less movement of cattle between counties were modelled. Scenarios with 20%, 40%, 60%, 80% and 100% fewer flocks sharing common pasture were modelled.
Scenarios with increased between county transmission
Increased between county movement of both sheep and cattle, and an increased number of flocks on common pastures are scenarios that we might see in the future. Hence the importance of this factor is highlighted. A five-fold and ten-fold increase was modelled.
Sensitivity analyses
By increasing and decreasing the basic scenario parameters one by one, an indication of the robustness of the model and the sensitivity of the model parameters is found. The sensitivity analysis was performed by stepwise increasing and decreasing of the parameters, starting with 80%, then 60%, 40% and 20%. The analysis was continued until the number of infected flocks did not deviate by more than 5% compared to the basic model. Thus, only the 80% increase and decrease was performed for the parameters which showed little variance in the results compared to the basic scenario. The parameters included in the sensitivity analysis were the infection rate, recovery rate, reversion rate, climatic value, climatic rate on common pasture, number of farms within 1 km (neighbouring flocks) and number of farms within 3 km (isolated flocks).
Model simulations
The model was run from 2005 and 30 years onward. In addition, the basic scenario where the time interval was extended to the year 2100 was made. The intention was to capture the percentage of flocks in each of the compartments when the equilibrium state was reached. The model was run using R v2.15.1 [20] and the additional package deSolve [21]. For each simulation of a scenario, 2000 replicates were made.
Results
Basic scenario
After the initial introduction of infection into a county, the model estimates that it takes four to twenty years before approximately 5% of the sheep flocks in the county are infected. Thereafter, one to nineteen years elapses before more than 30% of the sheep flocks in the county are infected. The steepest increase in the number of infected sheep flocks is observed in the five counties Rogaland, Hordaland, Vest-Agder, Sogn og Fjordane and Møre og Romsdal. Infected flocks in these counties increase from 5% to 60% within two to five years, while in the other counties it takes from eight to more than twenty years to reach this percentage (Figure 3).The counties of Rogaland and Finnmark have the highest and lowest percentages of infected flocks in 2100, at 88% and 7%, respectively, when the county of Oslo is excluded (0%). A state of equilibrium between the compartments are reached in the year 2068, when the number of infected flocks and low susceptible flocks stabilises at 76% and 24%, respectively.
Scenarios with different control measures
Scenarios with increased between county transmission
A ten-fold increase in the movement of sheep, the movement of cattle, and the use of common pasture increase the number of infected flocks in 2035 by 3%, 9% and 17%, respectively. The spread of severe footrot is further extended (compared to the basic scenario) to the county of Troms in the scenarios with increased movement of cattle and increased use of common pasture, and also to the county of Oslo in the scenario with increased movement of cattle.
Sensitivity analysis
Discussion
A simulation model is a useful tool to predict the spread of disease in a population. But spread of an infectious disease is a complex phenomenon with many interacting factors. Hence the development of a model must be based on knowledge of the specific disease in question and the routes of spread within the population as the model assumptions and the input variables used are important for obtaining a reliable result.
Most of the assumptions and input variables in this study have been based on observed parameters of the population, management and climate in Norway. In addition, the infection rate was based on observed values of the spread of footrot in Rogaland from introduction in 2005 until implementing the elimination program in 2009, and then adjusted to the other counties in Norway by using the observed spread in Aust-Agder. Data on spread for more than four years and more than two counties would have been desirable, but since an elimination program was implemented in Norway, such data was not available.
The sensitivity of the input parameters has also been examined. The variables found important in the sensitivity analysis were changes in the climatic value, the number of neighbouring flocks, the recovery, and the reversion rate. As expected, the climatic value is an important parameter for the spread of footrot. The values used in the model were based on observed mean precipitation and temperature for a 30 year period. More than a 20% increase or reduction of the observed value is not expected. Hence up to 14% decrease or 9% increase in the number of infected flocks compared to the basic scenario might be possible. The number of neighbouring flocks is also an important parameter. This value was based on the geographical coordinates of sheep farms. A higher or lower density of sheep farms might be possible, but we do not expect more than 20% change in this factor during the modelled 30 years. This would result in less than 5% deviation compared to the basic model. The recovery rate was based on data from the Healthy Feet project, and an increase or decrease in this value of more than 20% is not expected. With an increase/decrease of 20% the deviation from the basic scenario was less than 5%. The reversion rate is an important model parameter, and data on this value would have been desirable, but this is one of the few parameters in the model for which no data is available. A 40% change in this variable gives a more than 5% deviation in the result compared to the basic scenario. We cannot exclude the possibility that the reversion rate can have other values than the ones modelled. Low reversion rate is an advantage, and this can be achieved by good biosecurity measures. The rest of the variables did not change the outcome in the sensitivity analysis.
The reliability of the model can be assessed by comparing the infection dynamics in the model with what is expected based on knowledge of the disease and the spread in other populations.
Severe footrot was not introduced into the two northernmost counties in Norway in the period covered by the simulation. These counties are situated far from the county of Rogaland and to reach them the infection would have to cross several county borders that act as barriers for the transmission of the infection. In addition, the average temperature decreases going north in the country, resulting in a climate that is less favourable to the spread of footrot. A delayed introduction and spread to these counties, as predicted by the model, would accordingly be expected.
Another of the factors which increase the reliability of the model is the fact that the steepest increase in number of infected sheep flocks was seen in five counties that are all characterized by having a wet, warm climate and a relatively high density of sheep flocks compared to the other counties in Norway. These factors are known to enhance the development and spread of D. nodosus, resulting in a high within county infection rate, hence a steep increase is expected.
We also compared the modeled results with parameters from the UK, where footrot is endemic. In a study, 86% of the sheep farmers in the UK reported to have footrot within a twelve-month period, and more than 95% had experienced footrot at some time [22]. This is similar to the situation in Rogaland county which stabilised at 88%. The overall prevalence of infected flocks in Norway stabilised at a lower level, but this was as expected since the other counties with the exception of Hordaland, have a climate less favourable for footrot (Table 2).
Even though this model was based on the factors specific for Norway, a similar approach can be used to predict the spread of disease in other populations by estimating the input variables specific to the disease and the country or region in question.
Basic scenario
Extensive spread of severe footrot, in terms of both the number of infected flocks and the number of counties affected is predicted within 30 years (Figures 2, 3 and 4). This results in a large proportion of the Norwegian sheep population being affected by pain, lameness and welfare problems which would have a high economic cost for the sheep industry [23]. A comparison of the predicted number of infected flocks with the cumulative number of flocks diagnosed with severe footrot in 2013 appears to show that the footrot elimination programme initiated in 2009 was highly effective. This shows the importance of early implementation of an elimination programme for a newly introduced disease like severe footrot.
Scenarios with different control measures
The most effective way to reduce the spread of severe footrot was by decreasing the within county infection rate (Figure 5). This could be achieved by reducing contact between flocks or by reducing the environmental load of virulent D. nodosus, for example by footbathing, culling diseased sheep or eliminating severe footrot from the flock. In the event of an extensive outbreak of severe footrot, we believe that some farmers would implement control measures to reduce the welfare problem in their flock. A 20% or possibly a 40% decrease in the infection rate might be realistic, which would decrease the number of infected flocks in 2035 by 11% and 28%, respectively, compared with the basic scenario where no control measures are included.
The exclusion of one of the between counties transmission routes at a time, keeping the other two routes in the model, resulted in only a small decrease in the number of infected flocks in 2035. When two of the three transmission routes were excluded, a larger reduction in the number of infected flocks in 2035 was seen. When sheep movement was the only between county transmission route, the number of infected flocks decreased by 20%. Of the between county transmissions, this was the scenario with the largest deviation from the basic scenario. The low number of sheep moved across county borders is the main reason why the spread of disease is slowest for this route. National maedi and scrapie legislation prohibits the movement of sheep across county borders without derogation. This shows that keeping this transmission route only in the model at the current level limits the spread. This reflects the importance of the legislation in decreasing the spread of disease across county borders. With no such legislations, more sheep would be moved across the county borders and the spread of sheep diseases to other counties would be faster. The sheep industry in Norway supports the derogations for moving sheep across county borders, hence an increase is not expected.
Scenarios with increased between county transmission
Increased use of common pasture and movement of cattle gave the highest increase in the number of infected flocks of the between county transmissions. This shows the importance of the risk of spreading severe footrot by these means. But an extensive increase in these routes of transmissions is not expected as they are not restricted with legislations, and therefore not a major concern for the control of footrot in Norway.
The county-specific infection rates were based on the spread of severe footrot in Rogaland and adjusted to other counties by taking account of differences in climate and sheep density. The adjustment factors were fitted to the spread in Aust-Agder. We cannot exclude the possibility that other ways of generating the correction factors would be better. In view of the importance of the model results, data to validate the adjustment factors would have been beneficial, but such data does not exist for Norway.
In conclusion, a simulation model is a useful tool to estimate the spread of an infectious disease, but care must be taken so that model assumptions and values used are reasonable as the results are highly dependent on these. By using sensitivity analysis and assessing the consistency with spread in other populations, the reliability of the model can be assessed.
The spread of severe footrot in Norway without an elimination programme would have been extensive. Control measures decreasing the within county infection rate would delay the spread, but a ban on a single of the between county infection routes would not reduce the spread substantially. This shows the large effect, and the importance of initiating an elimination programme to prevent a large proportion of the Norwegian sheep population from being faced with pain, lameness and welfare problems. We cannot exclude the possibility of disease being introduced and spread by other means than those modelled, but we do believe that the model predicts a possible scenario for how the disease would develop in Norway without an elimination programme.
Declarations
Acknowledgements
The authors would like to thank the Healthy Feet project for providing access to their data. We would also like thank Malin Jonsson and Chiek Er at the Norwegian Veterinary Institute for their technical support. The project was funded by the Research Levy on Agricultural Products, project number 199142/199.
Authors’ Affiliations
References
- Beveridge WIB (1941) Foot-rot in sheep: a transmissible disease due to infection with Fusiformis nodosus. Studies on its cause, epidemiology and control. Council Sci Industr Res 140:1–56Google Scholar
- Wassink GJ, King EM, Grogono-Thomas R, Brown JC, Moore LJ, Green LE (2010) A within farm clinical trial to compare two treatments (parenteral antibacterials and hoof trimming) for sheep lame with footrot. Prev Vet Med 96:93–103View ArticlePubMedGoogle Scholar
- Ley SJ, Waterman AE, Livingston A, Parkinson TJ (1994) Effect of chronic pain associated with lameness on plasma cortisol concentrations in sheep: a field study. Res Vet Sci 57:332–335View ArticlePubMedGoogle Scholar
- Palmer MA (1993) A gelatin test to detect activity and stability of proteases produced by Dichelobacter (Bacteroides) nodosus. Vet Microbiol 36:113–122View ArticlePubMedGoogle Scholar
- Meling S, Ulvund MJ. Flock health visits in 17 sheep flocks in Rogaland. In Proceedings of the 7th International Sheep Veterinary Congress: 12–16 June 2009; Stavanger. Edited by Stuen S, Ulvund MJ: 2009;148–49.Google Scholar
- Øverås J (1994) Smittsom klauvsjuke hos sau. Et tilbakeblikk på import og utbrudd i Norge. Småfenytt 14:29–33 (in Norwegian)Google Scholar
- Vatn S, Hektoen L, Høyland B, Reiersen A, Kampen AH, Jørgensen HJ (2012) Elimination of severe footrot from the Norwegian sheep population - A progress report. Small Ruminant Res 106:11–13View ArticleGoogle Scholar
- Healthy Feet Project: Statusrapport nr. 6 Friske føtter. Oslo: Animalia, Norwegian Meat and Poultry Research Centre; 2014. [http://www.fotrate.no/media/_Statusrapport_nr_6_Friske_fotter_endelig_mars_2014.pdf] Accessed 07 July 2014.
- Gilhuus M, Vatn S, Dhungyel OP, Tesfamichael B, L’Abee-Lund TM, Jørgensen HJ (2013) Characterisation of Dichelobacter nodosus isolates from Norway. Vet Microbiol 163:142–148View ArticlePubMedGoogle Scholar
- Gilhuus M, Kvitle B, L’Abée-Lund TM, Vatn S, Jørgensen HJ (2014) A recently introduced Dichelobacter nodosus strain caused an outbreak of footrot in Norway. Acta Vet Scand 56:29View ArticlePubMed CentralPubMedGoogle Scholar
- de Jong MCM (1995) Mathematical modelling in veterinary epidemiology: why model building is important. Prev Vet Med 25:183–193View ArticleGoogle Scholar
- Rohani P, Earn DJ, Grenfell BT (1999) Opposite patterns of synchrony in sympatric disease metapopulations. Science 286:968–971View ArticlePubMedGoogle Scholar
- Grøneng GM, Green LE, Kaler J, Vatn S, Hopp P (2014) A longitudinal study of the risks for introduction of severe footrot into sheep flocks in the south west of Norway. Prev Vet Med 113:241–248View ArticlePubMedGoogle Scholar
- Nieuwhof GJ, Conington J, Bishop SC (2009) A genetic epidemiological model to describe resistance to an endemic bacterial disease in livestock: application to footrot in sheep. Genet Sel Evol 41:19View ArticlePubMed CentralPubMedGoogle Scholar
- Graham NPH, Egerton JR (1968) Pathogenesis of ovine foot-rot: the role of some environmental factors. Aust Vet J 44:235–240View ArticlePubMedGoogle Scholar
- Ridler A, Wilson D, Nixon N (2009) Effect of environmental and climatic conditions on footrot in sheep in the UK. In: Stuen S, Ulvund MJ (ed) Proceedings of the 7th International Sheep Veterinary Congress. Stavanger, Norway, pp 104–105Google Scholar
- Ghimire SC, Egerton JR, Dhungyel OP (1999) Transmission of virulent footrot between sheep and goats. Aust Vet J 77:450–453View ArticlePubMedGoogle Scholar
- Knappe-Poindecker M, Gilhuus M, Jensen TK, Vatn S, Jørgensen HJ, Fjeldaas T (2014) Cross-infection of virulent Dichelobacter nodosus between sheep and co-grazing cattle. Vet Microbiol 170:375–382View ArticlePubMedGoogle Scholar
- Rogdo T, Hektoen L, Slettemeås JS, Jørgensen HJ, Østerås O, Fjeldaas T (2012) Possible cross-infection of Dichelobacter nodosus between co-grazing sheep and cattle. Acta Vet Scand 54:19View ArticlePubMed CentralPubMedGoogle Scholar
- R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.Google Scholar
- Soetaert K, Petzoldt T, Setzer RW (2010) Solving differential Equations in R: package deSolve. J Stat Softw 33:1–25Google Scholar
- Wassink GJ, Grogono-Thomas R, Moore LJ, Green LE (2003) Risk factors associated with the prevalence of footrot in sheep from 1999 to 2000. Vet Rec 152:351–358View ArticlePubMedGoogle Scholar
- Nieuwhof GJ, Bishop SC (2005) Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Anim Sci 81:23–29View ArticleGoogle Scholar
Copyright
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.