No long-term influence of movement restriction regulations on the contact-structure between and within cattle holding types in the Netherlands
© Brouwer et al.; licensee BioMed Central Ltd. 2012
Received: 29 September 2010
Accepted: 3 October 2012
Published: 11 October 2012
More and more countries hold databases on cattle movements. The primary purpose of the registration of cattle movements is to provide data for quick tracing of contagious animals in case of disease outbreaks and food safety scares. Nevertheless, these data can also be used for analytical studies to get insight into the nature of the contact structure between and within cattle holding types. This paper focuses on the effect post-2001 FMD movement regulations have had on the number of cattle movements between different and within the same cattle holding types. Important characteristics and dynamics of cattle movement patterns of Dutch cattle holding types were identified using data on cattle movements after the 2001 FMD outbreak.
The results showed that in 2001, just after the FMD outbreak when strict movement restriction regulations were in force, a reduced number of cattle movements was seen compared to before the FMD outbreak. However, the number of cattle movements off-farm for live trade and the number of imported cattle increased in the period 2002–2004 to higher levels than expected, i.e. to levels almost as high as before the FMD outbreak, despite operative movement restriction regulations. As the number of cattle movements to and from traders strongly decreased just after the FMD outbreak in 2001, traders regained their central role again in the network in the years 2002–2004.
Quantifying the Dutch cattle contact structure between and within holding types up to 3.5 years after the FMD outbreak gave evidence that the post-FMD movement restriction regulations were not able to reduce the number of cattle movements in the longer term. With that the risk of a large epidemic increased. Quantifying contact structures based on animal movement data between different and within the same cattle holding types is important for targeting disease control and for assessing compliance with legislation.
Contacts between farms via cattle movements are considered to be an important risk factor in the spread of infectious diseases within and between animal holdings. Movement control and tracing of infections are among the first actions taken by veterinary authorities during disease outbreaks. To enable such measures, a registration system of cattle movements is crucial. Consequently, many countries have established authorities to register cattle movements, examples are the Cattle Tracing System in the UK , the National Livestock Identification System in Australia , the Central Husbandry Register (CHR) and Central Cattle Register (CKR) in Denmark , the Livestock Ranch Official Certification Program in Chile  and the Identification and Registration System in the Netherlands . Increasingly, the mandatory reporting of cattle movements between holdings are used by researchers for mathematical modelling to investigate the spread of for example food-and-mouth disease (FMD) [6–8] and scrapie . In addition, in the UK and Denmark movement data have been used to describe contact structures between cattle, pig or sheep holdings [8–10] to define risk-potential networks. This provides valuable information on the possibilities of disease transmission in the period between introduction and detection of infection. In addition, the efficacy of movement restriction regulations can be determined in the short and long term [11, 12].
After the end of the 2001 FMD outbreak in the Netherlands (on June 25th 2001) some of the movement restriction regulations were retained to reduce the number of cattle movements and, consequently, decrease the risk of transmission of infectious diseases in the future. The first regulation prohibited the gathering of cloven-hoofed animals for a period shorter than 30 days . The second regulation prohibited the movement of cloven-hoofed animals off-farm within 30 days after a cloven-hoofed animal had been moved on-farm . In May 2003, these regulations were eased to 21 days for all holding types instead of 30 days. These regulations made trading cattle for farmers more restrictive and complex. An exception to this rule were the markets and so-called cattle collection centres, where cattle were gathered for distribution to Dutch farmers or for export. These centres and markets were not allowed to gather cattle until June 2001. After June 2001, it was allowed to gather cattle in markets and collection centres on a daily basis given that strict hygiene protocols were met.
Velthuis and Mourits  used the I&R-database to compare the contact structure of the Dutch cattle industry before and immediately after the FMD outbreak. They concluded that due to the above mentioned regulations, the number of cattle movements off-farm for live trade had been reduced significantly in the year after the FMD outbreak and with a distinct change in the overall contact structure between and within holding types. Especially the number of cattle movements from dairy holdings to cattle collection centres was strongly decreased, whereas an increase in the number of cattle movements from dairy to beef holdings was seen. These changes were supposed to result in a reduction in size of epidemics. However, in the UK it was demonstrated that despite movement restriction regulations, the potential for large epidemics in the British cattle population has increased in the long term .
Due to differences in the cattle contact structure and regulations between countries, it was unknown how farmers outside the UK have adapted their cattle movements to threats imposed by highly contagious diseases. These differences could also have a different impact on holding owners“ responses to these movement restriction regulations. Because the European Union is a free trading zone, the national contact networks of the member states are interconnected. Therefore, it is important to quantify differences in contact structures between countries.
Definitions of cattle holding types in the Netherlands
Moving at least 20 animals on- and off-farm per year with a mean time present ≤ 60 days (including dealers, cattle shows, markets and cattle collection centres)
Young stock raising holdings
Holdings that raise young stock for dairy holdings
Holdings keeping calves for veal production and/or bulls for bull meat production
Suckling cow holders
Holdings keeping suckling cows
Holdings that have on average 20 animals or less present in a year
Holdings keeping dairy cows for milk production
Since we only used anonymous data from existing databases no informed consent from the holding owners was required.
Description of identification and registration (I&R) database
In the Netherlands, each cattle holding is obliged to report every cattle transport, birth or death to the national Identification and Registration (I&R) organisation. Each notification in the I&R-database consists of a unique farm identity number (UFI) related to one specific holding, an identification number of an animal, the birth date of the animal, the move on-farm code (birth, move on-farm, import) and move off-farm code (move off-farm for live trade, slaughter, death, export) and date of the movement. In this study, all cattle movement data from the Dutch I&R-organisation between July 2001-December 2004 were used.
Applications of the I&R database
First, the I&R-database was used to define holding types and to distinguish different types of cattle movements. Second, cattle movements between cattle holdings after the FMD outbreak were determined and compared with cattle movements before the FMD outbreak  to explore if cattle holding owners' responses to movement restriction regulations were different in the longer term (2002–2004) as compared to the short term (July-December 2001). In addition, the number of cattle movements between and within holding types was quantified over time and network features were determined per holding type.
Definition of holding types
Each year a cattle holding was given one of six holding types (Table 1). The average number of animals present in one calender year was calculated and divided into three age classes (<1 year old, 1–2 years old and >2 years old) using the move on-farm, move off-farm and birth dates from the I&R-database. In addition, the number of births and the number of animals that moved on-farm and off-farm in a year with their mean time present on the farm were determined. Based on these data and the mean proportions of male and female animals present on the farm, pre-established definitions  were used to define the holding types.
Types of cattle movements
From the I&R-database five types of cattle movements were distinguished: 1) off-farm for live trade, 2) off-farm for slaughter, 3) off-farm to the rendering plant for destruction, 4) off-farm for export and 5) import.
An animal movement off-farm for live trade consisted of linking two notifications with the same unique animal identification number. Only movements for which the off-farm movement could be traced forward to an on-farm movement within a 14-days period were selected for the analyses . Animals that were moved off-farm for slaughter, destruction or export or moved on-farm by import were defined as such in the database.
Cattle movements before and after the FMD outbreak
The mean number of cattle movements per month per year was determined for each movement type in the study period July 2001 to December 2004. In 2001, the after FMD period consisted of six months (July-December). Therefore, for each year only cattle movements in the period July-December were used to be able to compare cattle movements across years (i.e. to correct for seasonal effects). In addition, these numbers were compared with the mean number of cattle movements determined in the period before the FMD outbreak from July to December 2000  to quantify the effect of the retained movement restriction regulations after the FMD outbreak. Differences in the mean number of cattle movements between years were tested, using a Kruskal-Wallis multiple comparison test (P ≤ 0.05).
Cattle movements between and within holding types
For the transmission of diseases within the Netherlands, cattle movements off-farm for live trade were considered as potentially risky contacts, in contrast to movements to slaughterhouses, to the rendering plant or abroad. The mean number of cattle movements off-farm for live trade per month was determined to quantify the contacts between and within Dutch cattle holding types for each year. For the identification of possible changes in the contact structure in the long term, for each year only cattle movements in the period July-December were used to be able to compare cattle movements off-farm for live trade across years.
The contact structure between and within holding types was visualized with the program UCInet (Analytic Technologies, Harvard, MA) for the years 2001 and 2004 to illustrate the change from 2001 to 2004. The data were represented as a network with six nodes (holding type) and edges representing the number of cattle movements between the nodes per year. Within node movements were represented by loops . For a clear visual presentation of contact structures, only cattle movements between and within holding types with a minimum of an arbitrary number of 1,000 cattle movements per month were shown.
The number of animals that move on-farm (i.e. open/closed farming system) in the last 12 months
The mean percentage of holdings with off-farm movements in a month
The number of different holdings an UFI has contact with (degree) per month
The number of contacts with the same holding per month
The number of animals moved per contact per month
Direct distances of cattle movements between holdings
The network features ‘mean percentage of holdings with off-farm movements', ‘holding contacts’ and ‘direct distances’ were based on off-farm movements for live trade, because these movements were considered as risky contacts.
Closed holding system
For each quarter the number of animals that were moved on-farm in the last 12 months was calculated. Based on this number, each UFI was set to an open (at least one animal moved on-farm in the last 12 months) or closed (no animals moved on-farm in the last 12 months) holding system per quarter (q1 = January-March; q2 = April-June; q3 = July-September; q4 = October-December). We could determine whether a holding was set to a closed holding system from July 2002 on, because on an earlier date the FMD period would be included in the definition for a closed holding system.
Calculation of the distance
For each holding type, the direct distance for all movements off-farm for live trade per month was estimated. Therefore, x and y co-ordinates for each UFI were used (source; GD, Animal Health Service Ltd., Deventer). If (x1, y1) are the co-ordinates of the UFI moving animals off-farm and (x2, y2) are the co-ordinates of the UFI moving animals on-farm, the Euclidean distance between two holdings was calculated. To compare Euclidean distances between holding types, these distances were divided in two categories: 0–40 km and >40 km.
Cattle movements before and after the FMD outbreak
The mean number of cattle movements (*10 3 ) per month before FMD (2000) and after FMD (2001–2004) in the Netherlands
Cattle movement type
Off-farm for live trade
Off-farm for slaughter
Off-farm for destruction
Off-farm for export
Cattle movements between and within holding types
Description of on-farm and off-farm movements for different cattle holding types in the Netherlands from July 2001 to December 2004
Percentage closed herds in previous 12 months
Percentage of cattle movements off-farm for life trade
Percentage farms with contacts in one month
Degree (No. of different contact farms in one month)
No. Contacts with same farm in one month
No. of animals moved/contact in one month
Young stock raising farms
Suckling cow holders
Closed holding system and holding contacts
The analyses carried out in this study identified important characteristics and dynamics of cattle movement patterns between and within cattle holdings across years. With these analyses, the efficacy of movement restriction regulations was determined in the short (up to one year) and long (up to 3.5 years) term. Our results acknowledged what has previously been reported by Velthuis and Mourits  and showed that trading cattle strongly decreased just after the FMD outbreak (2001). This change was especially seen in the strong decline of cattle movements off-farm for live trade and the decreased import of animals by traders. However, our study also showed a subsequent increase of the number of cattle imports and movements off-farm for live trade in the years 2002–2004 despite retained movement restriction regulations after the 2001 FMD outbreak. This increase was higher than expected as the number of these movements was practically as high as before the FMD outbreak. Traders regained their central role again in the network and the number of traders increased more than two-fold from 160 in 2001 to 374 in 2004. It was assumed that holding owners enforced the rules, because when they violated the rules, a blockade was imposed on their holding. Quantifying the Dutch cattle contact structure between and within holding types up to 3.5 years after the FMD outbreak gave evidence that the post-FMD movement restriction regulations were not able to reduce the number of cattle movements in the longer term. Obviously, the fear of farmers for introduction of FMD and culling of cattle has temporarily changed the cattle contact structure. Similar results were found in the UK . They used a more complex network analysis on holding level to determine the efficacy of movement restriction regulations over time. Our study showed, that using simple network features on holding type level produced the same results. However, in our study design the variation between individual holdings in the movement network and the impact of those cattle holdings on the transmission of diseases is unknown. Other studies have shown that the identity of individual holdings responsible for making network connections can have a significant impact on the infection dynamics [8, 16, 17]. However, our study focused on network connections between holding types because different holding type authorities exist in the Netherlands that design and enforce type-specific regulations.
The reduced efficacy of the movement restriction regulations can increase transmission of diseases between holdings. Therefore, quantification of the contact structure at any time is essential to assess the compliance with legislation. The effect of the movement restriction regulations in this study was assessed by the change in the contact structure between and within holding types. However, other regulations and economic drive, such as cattle prices, may also have affected the contact structure. However, no evidence exists of a major drive that could have affected the contact structure in the years 2001 to 2004 and therefore the impact on our analyses is considered not serious or even negligible.
As more and more countries hold databases on cattle movements, the analyses that were carried out in this study could also be performed on data concerning cattle movements in other countries. A possible situation may arise that despite movement restriction regulations, the contact structure changes in such a way that the risk of transmission of diseases between holdings increases more than expected and is also present in other countries.
This study also showed that the contact structure between and within Dutch cattle holding types was not random. For example, we found that most dairy holdings had contacts with beef holdings every month. As Dutch dairy holdings have no specific calving season, these movements are due to the off-farm movements of bull calves for beef-rearing and female calves for young stock raising. In addition, despite the small numbers, traders (incl. shows, markets and collection centres) played a central role in the network in the years 2002–2004. Many cattle holdings are connected by movements to and from traders, which are often mixing animals from different holdings. The mixing of animals has been suggested as an important factor in disease dissemination . Moreover, our study showed that movements from traders frequently occurred over long distances. As a result, diseases can easily spread to other areas. In other studies about contact networks between cattle holdings and between swine holdings, a similar non random contact structure was seen [9, 10, 18]. Data describing contact structures between holding types can be very useful for epidemiological studies on the spread of animal diseases. However, in many mathematical models on disease transmission it is assumed that contacts between and within holding types are random, while in reality this is not the case. This assumption is especially not valid when it comes to crisis management. In most cases only particular individual cattle holdings are an important risk factor in the transmission of diseases . The use of heterogeneous contact parameters has shown to describe animal movement data better than random contact parameters . In addition, Dickey et al.  stated that the use of heterogeneous contact parameters predict the transmission of FMDV more accurately than random contact parameters. Moreover, Vernon and Keeling mentioned that due to temporal structures within the dynamic network, static networks consistently fail to capture the predicted epidemic behaviour associated with dynamic networks and therefore recommend to use dynamic networks . Therefore, for efficient disease control it is very important to quantify non-random factors in the contact structure to provide a better understanding of disease transmission. In addition, it allows more realistic comparison of control strategies in case of disease modelling.
Census data from the Dutch Identification and Registration organisation were used to describe the contact structure of the Dutch cattle industry. In the Netherlands, farmers are obliged to report cattle movements. However, compliance is unknown and there can still be some bias in the data due to errors or omissions in the numbers and type of stock moved. In addition, movements of trucks that carry out animal transfers are not available in this database, whereas these trucks could also be an important risk factor for the transmission of diseases. Moreover, other potential transmission routes like the movements of equipment, wildlife and personnel were not included in the I&R database. These biases could underestimate the number of cattle movements between herds of the same and different herd types and with that the risk of disease transmission between cattle herd types. Despite these biases, the database includes detailed information on all cattle movements in the Netherlands over several years. Since there is no evidence that these biases are unevenly dispersed over the years, we think that the biases will probably have a minor impact on our analyses. Acknowledging the limitations, which are also present in other countries like the UK, we believe that the analyses provide useful information on cattle movement patterns in the cattle industry. This knowledge can be important in the early phase of a disease outbreak by providing a better focus on tracing activities .
Quantifying the Dutch cattle contact structure between and within holding types up to 3.5 years after the FMD outbreak gave evidence that the post-FMD movement restriction regulations were not able to reduce the number of cattle movements in the longer term. With that the risk of a large epidemic increased.
The analyses provide useful information on cattle movement patterns, which can be important for targeted disease control and for assessing compliance with legislation. This information can be important in the early phase of a disease outbreak, by providing a better focus on tracing activities and disease modelling. Further research is necessary to determine the variation between individual holdings in the movement network and the impact of those cattle holdings on the transmission of diseases.
This study was carried out in the framework of the Dutch Cattle Health Monitor from the Animal Health Service Ltd, Deventer, the Netherlands. We thank the Dutch Dairy Commodity Board and the Dutch Ministry of Agriculture, Nature and Food Quality for funding this study. We also like to thank Annet Velthuis for her useful input in this study.
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