GLOWORM-META: Modelling gastrointestinal nematode metapopulation dynamics to inform cattle biosecurity research

Gastrointestinal nematode (GIN) parasite infections in grazing livestock cause significant disease, and are responsible for estimated annual losses of over {euro}1.8 billion in Europe alone. The management of GINs in cattle is threatened by anthelmintic drug resistance (AR). Immediate action is needed to slow the progression of AR in cattle GINs and avoid the increasingly common scenario of multiple drug resistance seen in sheep. Although AR can arise independently on multiple farms, it may also be spread between holdings via purchased cattle. Therefore, effective biosecurity measures on cattle enterprises could help to reduce the risk of establishment of AR populations. A metapopulation model was developed and validated for two GIN species infecting cattle, Ostertagia ostertagi and Cooperia oncophora, incorporating the full parasite life cycle, weather- and immunity-dependent parasite life history traits and multiple pasture sub-populations. This allowed for complex grazing management strategies and weather influences to be simulated. The models successfully replicated the seasonal patterns and intensity of infections reported in multiple published longitudinal datasets. Global sensitivity analysis against four Quantities of Interest (QoIs) related to factors affecting the safety of the resident herd and of the purchased animals was used to quantify the influence of candidate biosecurity measures. The duration of quarantine, the date of purchase (weather/seasonal influences) and the intensity of infection on the day of purchase strongly influenced the QoIs. The outcomes for the UK were not significantly influenced by the geographic location of the purchasing farm, suggesting that the influence of weather patterns on GIN populations outweighs that of regional climate differences, and thus regional variations to GIN biosecurity recommendations are not warranted without alternative evidence to support this. The model presented here is the first full lifecycle GIN metapopulation model for O. ostertagi and C. oncophora, validated against longitudinal field data, and can be broadly used to evaluate the relative efficacy of a range of cattle GIN management strategies, as demonstrated here. These findings offer valuable insights to focus initial biosecurity recommendations for cattle enterprises, and are being used to direct qualitative and quantitative research to refine recommendations. HighlightsO_LIA metapopulation model for cattle GINs was developed C_LIO_LIThe model includes weather-dependence and complex grazing C_LIO_LIThe model replicated seasonal infection patterns from multiple datasets C_LIO_LISensitivity analysis explored influential biosecurity measures C_LIO_LIThe influence of weather outweighed that of geographic location (climate) C_LIO_LIInitial recommendations for biosecurity and further research are made C_LI