Development of a transmission model for gastro-intestinal nematode infections in cattle

Gastro-intestinal nematodes (GIN) are one of the great threats for farmed ruminants worldwide. Mathematical models that simulate the dynamics of GIN infections have great potential to provide improved understanding of parasite epidemiology under altered conditions and to underpin the development of alternative parasite control strategies. In chapter 1, first the general epidemiology of GIN in ruminants is discussed to provide insight in the dynamics and underlying drivers of the host-parasite interaction. Host immunity, weather and farm management are shown to be significant drivers of parasite epidemiology. The second part of chapter 1 discusses the evolution of both hosts and parasites during the past half century, the expected trends to come and the underlying drivers of these anticipated changes. Finally, the value of transmission models to improve our understanding of parasite epidemiology under changing conditions and to facilitate the development of control strategies is discussed. Key terms encountered in the field of parasitic disease modelling are explained and the development process of these models is given. An overview of the available models for GIN infections in ruminants provides insights into the needs for this field of research. The overall objective of this PhD project was to develop a generic framework for a mechanistic transmission model that simulates the parasitic phase of the GIN lifecycle in farmed ruminants. Further, facilitation of the collection of pasture larval count data, a key input parameter, was explored. Chapter 2 quantifies the main life history traits of the parasitic phase for O. ostertagi and Cooperia oncophora through systematic review and meta-analysis and assesses the potential influences associated with the effect of immunity on these traits. The main parameters determining parasite density during the parasitic phase are the larval establishment rate or pre-adult mortality, the hypobiosis rate, adult mortality and female fecundity. A systematic review was performed covering studies from 1962 to 2007, in which helminth-naïve calves were artificially infected with O. ostertagi and/or C. oncophora. The database was further extended with results of unpublished trials conducted at the Laboratory for Parasitology of Ghent University, Belgium. Overall inverse variance weighted estimates were computed for each of the traits through random effects models. To our knowledge, this systematic review is the first to summarize the available data on the main life history traits of the parasitic phase of O. ostertagi and C. oncophora and provides novel estimates for the parameterization of life cycle-based transmission models. Chapter 3 presents a flexible model framework (GLOWORM-PARA) developed for the parasitic phase of GINs infecting ruminants. The framework can be applied to a range of GIN species and is parameterised and thoroughly validated for first season grazing calves infected by two species that are of major importance in cattle, i.e. O. ostertagi and C. oncophora. To our knowledge, no previous attempt has been made to model C. oncophora. For O. ostertagi, GLOWORM-PARA incorporates important improvements to the existing models such as data-driven parameterisation of the rate of acquisition of immunity based on cumulative exposure and the incorporation of host grazing behaviour. Both the parameterisation and validation of these models were backed by extensive datasets obtained from various sources and acquired over decades of parasitological research. This represents the most comprehensive and thorough validation of GIN models to date. The model was able to generate the general patterns of faecal egg counts seen in first season grazing cattle throughout the grazing season. The estimation of the immune response rate from field observations was preferred over fitting the immune response rate to get meaningful predictions of acquired immunity. Linear regression of predictions against observations showed that incorporating host grazing behaviour resulted in an important improvement of model performance and is therefore likely to be important in the transmission of GIN. Assessing levels of pasture larval contamination is frequently used to study the population dynamics of the free-living stages of parasitic nematodes of livestock and the abundance of infective larvae (L3) on pasture is an important input parameter for GLOWORM-PARA. Direct quantification of L3 on herbage is the most applied method to measure pasture larval contamination, but herbage collection remains labour intensive. Chapter 4 compares two different sampling methods in terms of pasture larval count results and time required to sample, to assess the amount of variation in larval counts at the level of sample plot, pasture and season, respectively and to calculate the required sample size to assess pasture larval contamination with a predefined precision using random plots across pasture. Chapter 5 discusses the results and limitations of this work along with opportunities for future research. The integration of GLOWORM-PARA with a complementary model which simulates the free-living stages of GINs, GLOWORM-FL, should lead to a full life cycle based model in further research. To improve the link between the free-living and the parasitic phase, future research needs to assess the daily faecal production based on easy-to-use predictors such as body weight. The incorporation of a component that models grass growth can provide the needed complexity to account for different farm management situations and to underpin meaningful larval infection rates. Several questions remain concerning the implementation of transmission models as site-specific decision support tools for nematode control. A proposed approach to achieve better and more applied modelling is to gradually refine generic models with the needed amount of biological detail. Obtaining relevant and realistic parameter estimates and integrating these in generic models might be a good step to achieve the right balance between generality and specificity. Efforts to facilitate data quality and collection should be encouraged, as this is fundamental to make progress and underpins the future implementation of models. Future research should also focus on how to improve knowledge transfer to the end-users and to identify user-needs

Cattle and Nematodes Under Global Change:Transmission Models as an Ally

Nematode infections are an important economic constraint to cattle farming. Future risk levels and transmission dynamics will be affected by changes in climate and farm management. The prospect of altered parasite epidemiology in combination with anthelmintic resistance requires the adaptation of current control approaches. Mathematical models that simulate disease dynamics under changing climate and farm management can help to guide the optimization of helminth control strategies. Recent efforts have increasingly employed such models to assess the impact of predicted climate scenarios on future infection pressure for gastrointestinal nematodes (GINs) in cattle, and to evaluate possible adaptive control measures. This review aims to consolidate progress in this field to facilitate further modeling and application

Non-invasive indicators associated with the milk yield response after anthelmintic treatment at calving in dairy cows

Background: Gastrointestinal nematodes are an important cause of reduced performance in cattle. Previous studies in Europe showed that after anthelmintic treatment an average gain in milk production of around 1 kg per day/cow can be expected. However, (1) these studies have mainly evaluated group-based anthelmintic treatments during the grazing season or at housing and (2) little is known about parameters affecting variations in the treatment response amongst cows. A better knowledge of such parameters could help to select animals that benefit most from treatment and thus lead to a more rational use of anthelmintics. Therefore, a randomized, non-blinded, controlled clinical trial was performed on 11 commercial dairy farms (477 animals) in Belgium, aiming (1) to study the effect of eprinomectin treatment at calving on milk production and (2) to investigate whether the milk yield response was related to non-invasive animal parameters such that these could be used to inform targeted selective treatment decisions. Results: Analyses show that eprinomectin treatment around calving resulted in an average (+/- standard error) increase of 0.97 (+/- 0.41) kg in daily milk yield that was followed up over 274 days on average. Milk yield responses were higher in multiparous compared to primiparous cows and in cows with a high (4th quartile) anti-O. ostertagi antibody level in a milk sample from the previous lactation. Nonetheless, high responses were also seen in animals with a low (1st quartile) anti-O. ostertagi antibody level. In addition, positive treatment responses were associated with higher faecal egg counts and a moderate body condition score at calving (2nd quartile). Conclusions: In conclusion, this study provides novel insights into the production response after anthelmintic treatment at calving and factors which influence this. The data could be used to support the development of evidence-based targeted selective anthelmintic treatment strategies in dairy cattle

Review and Evaluation of Ostertagia ostertagi Antibody ELISA for Application on Serum Samples in First Season Grazing Calves

Simple Summary Gastrointestinal (GI) nematode infections are a significant health and welfare threat to calves in pasture-based rearing systems. Sustainable control requires an efficient and cost-effective diagnostic tool. The serum pepsinogen assay is a long-established tool to monitor the infection level. However, the relatively high cost and lack of standardisation hinder the broad implementation of this method. Here, the more cost-efficient and robust Ostertagia ostertagi-Ab ELISA is evaluated as a potential alternative diagnostic method in first-season grazing (FSG) calves. We performed both a literature review of studies where this method has been applied in FSG calves and conducted field studies in Belgium and Sweden to compare results from the O. ostertagi-Ab ELISA with the serum pepsinogen assay. We conclude that the O. ostertagi-Ab ELISA test is a valuable monitoring tool in FSG calves and could complement or replace the serum pepsinogen assay. The O. ostertagi-Ab ELISA assay is widely used as a diagnostic tool for monitoring gastrointestinal (GI) nematodes using milk samples from adult dairy cows. This assay is potentially also useful to analyse serum samples from first-season grazing (FSG) calves, providing a more cost-effective and robust diagnostic technique than the current serum pepsinogen assay. However, a comprehensive evaluation of its use in serum samples from FSG calves has not yet been conducted. In this study, we first reviewed the available scientific literature in which the O. ostertagi-Ab ELISA was applied to serum samples from FSG calves. Then, a field study was conducted to compare results from the O. ostertagi-Ab ELISA assay with a serum pepsinogen assay on a set of 230 serum samples from 11 commercial dairy herds (seven in Belgium and four in Sweden). The literature review showed an increase in mean antibody levels, expressed as optical density ratio (ODR) values, from <0.4 (early grazing season) to values of 0.7-1.1 (late grazing season). Three out of five studies found a negative correlation between O. ostertagi antibody levels measured during the late grazing season and weight gain, while the other two studies found no correlation between the two variables. Our field studies showed a good correlation between O. ostertagi antibody levels and the results from the pepsinogen assay. Both indicators were negatively related to average daily weight gain in the Belgian herds, but not in the Swedish herds. Overall, the results suggest that the O. ostertagi-Ab ELISA test can be a useful tool in FSG calves and could replace the use of the serum pepsinogen assay at the end of the grazing season for general monitoring purposes

Review and evaluation of ostertagia ostertagi antibody ELISA for application on serum samples in first season grazing calves

Simple Summary Gastrointestinal (GI) nematode infections are a significant health and welfare threat to calves in pasture-based rearing systems. Sustainable control requires an efficient and cost-effective diagnostic tool. The serum pepsinogen assay is a long-established tool to monitor the infection level. However, the relatively high cost and lack of standardisation hinder the broad implementation of this method. Here, the more cost-efficient and robust Ostertagia ostertagi-Ab ELISA is evaluated as a potential alternative diagnostic method in first-season grazing (FSG) calves. We performed both a literature review of studies where this method has been applied in FSG calves and conducted field studies in Belgium and Sweden to compare results from the O. ostertagi-Ab ELISA with the serum pepsinogen assay. We conclude that the O. ostertagi-Ab ELISA test is a valuable monitoring tool in FSG calves and could complement or replace the serum pepsinogen assay. The O. ostertagi-Ab ELISA assay is widely used as a diagnostic tool for monitoring gastrointestinal (GI) nematodes using milk samples from adult dairy cows. This assay is potentially also useful to analyse serum samples from first-season grazing (FSG) calves, providing a more cost-effective and robust diagnostic technique than the current serum pepsinogen assay. However, a comprehensive evaluation of its use in serum samples from FSG calves has not yet been conducted. In this study, we first reviewed the available scientific literature in which the O. ostertagi-Ab ELISA was applied to serum samples from FSG calves. Then, a field study was conducted to compare results from the O. ostertagi-Ab ELISA assay with a serum pepsinogen assay on a set of 230 serum samples from 11 commercial dairy herds (seven in Belgium and four in Sweden). The literature review showed an increase in mean antibody levels, expressed as optical density ratio (ODR) values, from <0.4 (early grazing season) to values of 0.7-1.1 (late grazing season). Three out of five studies found a negative correlation between O. ostertagi antibody levels measured during the late grazing season and weight gain, while the other two studies found no correlation between the two variables. Our field studies showed a good correlation between O. ostertagi antibody levels and the results from the pepsinogen assay. Both indicators were negatively related to average daily weight gain in the Belgian herds, but not in the Swedish herds. Overall, the results suggest that the O. ostertagi-Ab ELISA test can be a useful tool in FSG calves and could replace the use of the serum pepsinogen assay at the end of the grazing season for general monitoring purposes