Quantification of the contact structure in a feral cattle population and its hypothetical effect on the transmission of bovine herpesvirus 1

Abstract

The organisation of animal populations in social groupings may play a crucial role in the transmission of any infectious disease that requires close contact. The objective of this study was to quantify the contact structure of part of the Heck cattle population in a Dutch nature reserve and its hypothetical effect on the transmission of bovine herpesvirus 1 (BHV1). The contact structure was quantified by observing the number of different animals with whom contact was made (i.e. the number of contactees) within a fixed time period. Two types of behaviour sampling methods, namely focal sampling and scan sampling were used to observe the contact structure. In this study only those contacts between individuals were observed that were assumed to be a proxy measure of an at-risk event for BHV1-infection. Two reproduction ratios (R), i.e. the average number of new cases caused by a typical infected individual, were estimated, one for the observed contact structure and another for a random mixing contact structure. The two reproduction ratios were then compared to study the hypothetical effect on BHV1 transmission.

The overall number of contactees was highest during summer and lowest during winter-spring. The contact structure of the homogeneous population did differ significantly from a random mixing contact structure, resulting in that the variation in the number of contactees was higher than under random mixing. Bulls, young bulls and cows had the highest number of contactees during, respectively, summer, autumn and winter-spring. From the analysis of the contingency tables it was clear that contacts between animal types did not occur at random during summer and autumn. For example, during summer more contacts than expected occurred between bulls and cows. This heterogeneity at animal type level was taken into account in the calculation for R, which resulted for the observed contact structure in higher estimates for R than for the homogeneous population.

When looking at heterogeneity at individual level it was found that during summer almost all individuals were observed together direct or indirect in the same group except for certain bull groups. During autumn and winter-spring almost all individuals were seen together in the same group when considering a long contact period of 14 days but the groups were fallen apart in smaller groups and solitary individuals for a short contact period of 5 days.

It could be concluded that based on the observed contact structure transmission would be favoured most during summer.

Introduction

Many animal populations, such as bovines, live in social groupings (Sinclair, 1977) for part of the year (Lazo, 1994). The organisation of animal populations in social groupings may play a crucial role in the transmission of any infectious disease that requires close contact. For example when social groupings live isolated from each other during time periods longer than the period of disease outbreaks, the epidemic may be limited to the group in which the infection is started.

The animal population in this study is a population of Heck cattle (Van Vuure, 2005) – a crossbred from various races resembling the extinct aurochs Bos primigenius – living in a nature reserve in The Netherlands. The social organisation of the Heck cattle population was studied by Vulink (2001) from June 1991 until July 1992. Vulink (2001) described four social groups in the Heck cattle population namely: (i) solitary bulls; (ii) bull groups; (iii) cow groups; and (iv) mixed groups. The home range and the home range size of mature bulls and cow groups were studied. Mature bulls often stayed in small groups and only used a restricted part of the area. Cow groups on the other hand, consisted of large numbers of animals and moved among the home ranges of various bull groups. The differences between mature bulls and cow groups in home range size were always distinct and the differences in home range varied during the year, being greatest in winter (Vulink, 2001).

We were then interested in the influence of the social organisation of the Heck cattle population on disease transmission. The pathogen bovine herpesvirus 1 (BHV1) was chosen for this study because most (110 out of 124) of the above mentioned Heck cattle, that were tested in the period 1996–2003, were seropositive for BHV1 using a gB blocking ELISA. BHV1 is an alphaherpesvirus that infects cattle causing infectious bovine rhinotracheitis (IBR) and genital infections (Gibbs and Rweyemamu, 1977). This study focused on the subtype of BHV1 that causes IBR. If a susceptible individual is infected, the infectious individual may excrete the virus over a period of between 10 and 17 days (Wentink et al., 1993). Once the virus has infected an individual it remains in that individual for life. An individual that is already infected with BHV1 is called a latently infected individual. Latently infected individuals may re-excrete the virus under certain stress conditions (e.g. transport, parturition) but for a shorter time period than a primary infectious individual does (Wentink et al., 1993). Latently infected individuals that re-excrete virus may establish primary infections within susceptible animals in contact with the excreting animal. If not all latently infected individuals have died or have been taken out of that population before the infection is transmitted, BHV1 will persist in the population.

The objective of this study was to quantify the contact structure of part of the Heck cattle population in a Dutch nature reserve and its hypothetical effect on BHV1 transmission. We started with the observation and analysis of the contact structure. One of the observations was the number of different animals with whom contact was made, within a fixed time period. Heterogeneity at animal type level and at individual level were taking into account in the observation and analysis of the contact structure. Next, the method for calculating the potential for BHV1 transmission was described. The distribution of the number of different animals with whom contact was made, was used to calculate a reproduction ratio, which is defined as the average number of new cases caused by a typical infected individual (Diekmann et al., 1990). Reproduction ratios were calculated both for the observed contact structure and also for a random mixing contact structure. Random mixing was chosen as this type of mixing is predominantly used in epidemiological models. The two reproduction ratios were then compared to study the hypothetical effect of the actual observed contact structure on BHV1 transmission. This comparison was done because the absolute reproduction ratio could not be estimated. The hypothetical effects of the observed contact structure on BHV1 transmission and on the persistence of BHV1 were discussed.