Johannes Charlier

Gastrointestinal nematode infections in adult dairy cattle: impact on production, diagnosis and control.

Due to the intensification of dairy herds and the recognition of subclinical infections with a negative impact on production as disease, control of gastrointestinal (GI) nematodes in adult cows is becoming established in an increasing number of dairy herds. The objectives of this paper are to review the aspects related to the impact on production, diagnosis and control of GI nematodes in adult dairy cattle. During the last decade substantial evidence has been generated that GI nematodes can have a negative impact on the performance of adult animals. The milk-yield response to anthelmintic treatment in recent studies in pastured dairy herds was observed to be around 1kg/cow per day, whereas effects on reproductive performance remain equivocal. GI-nematode infections can be monitored based on Ostertagia ostertagi-specific antibody measurement, which provides information on the level of larval exposure and an indication of the associated production losses. Other diagnostic parameters are considered of limited use in adult cattle. Control relies on anthelmintic treatment and grazing management, which can be used complementary to each other. There are three critical points that need to be considered when developing anthelmintic control recommendations in adult cows: the unpredictability of the treatment response, the timing of treatment and the risk for developing anthelmintic resistance. As a consequence, monitoring of GI-nematode infections is desirable in order to focus anthelmintic treatments on those herds with a high larval challenge and associated production losses. For the future, more studies are needed to evaluate the effects of different control approaches in terms of financial benefits for the farmer and sustainability on the long term.

Chasing helminths and their economic impact on farmed ruminants

Global agriculture will be required to intensify production from a shrinking natural resource base. Helminth infections of ruminants are a major constraint on efficient livestock production. The current challenge is to develop diagnostic methods that detect the production impact of helminth infections on farms in order to target control measures and contribute to the global challenge of preserving food security. We review here our understanding of the effects of helminth infections and control practices on productivity and the diagnostic tools that can inform on this. By combining advances in helminth laboratory diagnostics and animal health economics, sustainable management of helminth infections can be integrated into the whole-farm economic context.

A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths

Background The Kato-Katz thick smear (Kato-Katz) is the diagnostic method recommended for monitoring large-scale treatment programs implemented for the control of soil-transmitted helminths (STH) in public health, yet it is difficult to standardize. A promising alternative is the McMaster egg counting method (McMaster), commonly used in veterinary parasitology, but rarely so for the detection of STH in human stool. Methodology/Principal Findings The Kato-Katz and McMaster methods were compared for the detection of STH in 1,543 subjects resident in five countries across Africa, Asia and South America. The consistency of the performance of both methods in different trials, the validity of the fixed multiplication factor employed in the Kato-Katz method and the accuracy of these methods for estimating ‘true’ drug efficacies were assessed. The Kato-Katz method detected significantly more Ascaris lumbricoides infections (88.1% vs. 75.6%, p<0.001), whereas the difference in sensitivity between the two methods was non-significant for hookworm (78.3% vs. 72.4%) and Trichuris trichiura (82.6% vs. 80.3%). The sensitivity of the methods varied significantly across trials and magnitude of fecal egg counts (FEC). Quantitative comparison revealed a significant correlation (Rs >0.32) in FEC between both methods, and indicated no significant difference in FEC, except for A. lumbricoides, where the Kato-Katz resulted in significantly higher FEC (14,197 eggs per gram of stool (EPG) vs. 5,982 EPG). For the Kato-Katz, the fixed multiplication factor resulted in significantly higher FEC than the multiplication factor adjusted for mass of feces examined for A. lumbricoides (16,538 EPG vs. 15,396 EPG) and T. trichiura (1,490 EPG vs. 1,363 EPG), but not for hookworm. The McMaster provided more accurate efficacy results (absolute difference to ‘true’ drug efficacy: 1.7% vs. 4.5%). Conclusions/Significance The McMaster is an alternative method for monitoring large-scale treatment programs. It is a robust (accurate multiplication factor) and accurate (reliable efficacy results) method, which can be easily standardized.

Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone

Fasciola hepatica, a trematode parasite with a worldwide distribution, is the cause of important production losses in the dairy industry. Diagnosis is hampered by the fact that the infection is mostly subclinical. To increase awareness and develop regionally adapted control methods, knowledge on the spatial distribution of economically important infection levels is needed. Previous studies modelling the spatial distribution of F. hepatica are mostly based on single cross-sectional samplings and have focussed on climatic and environmental factors, often ignoring management factors. This study investigated the associations between management, climatic and environmental factors affecting the spatial distribution of infection with F. hepatica in dairy herds in a temperate climate zone (Flanders, Belgium) over three consecutive years. A bulk-tank milk antibody ELISA was used to measure F. hepatica infection levels in a random sample of 1762 dairy herds in the autumns of 2006, 2007 and 2008. The infection levels were included in a Geographic Information System together with meteorological, environmental and management parameters. Logistic regression models were used to determine associations between possible risk factors and infection levels. The prevalence and spatial distribution of F. hepatica was relatively stable, with small interannual differences in prevalence and location of clusters. The logistic regression model based on both management and climatic/environmental factors included the factors: annual rainfall, mowing of pastures, proportion of grazed grass in the diet and length of grazing season as significant predictors and described the spatial distribution of F. hepatica better than the model based on climatic/environmental factors only (annual rainfall, elevation and slope, soil type), with an Area Under the Curve of the Receiver Operating Characteristic of 0.68 compared with 0.62. The results indicate that in temperate climate zones without large climatic and environmental variation, management factors affect the spatial distribution of F. hepatica, and should be included in future spatial distribution models.

The use of bulk-tank milk ELISAs to assess the spatial distribution of Fasciola hepatica, Ostertagia ostertagi and Dictyocaulus viviparus in dairy cattle in Flanders (Belgium).

Fasciola hepatica, Ostertagia ostertagi and Dictyocaulus viviparus are helminth parasites with a wide distribution and an important economic impact in cattle in temperate climates. This paper describes the spatial distribution of F. hepatica, O. ostertagi and D. viviparus in dairy herds in Flanders (Belgium). One thousand eight hundred herds were selected at random from the Flemish dairy population (n=7002), stratified on community level to obtain a sample representative for the entire study area. From each herd, a bulk milk sample collected in autumn 2006 was analysed with previously described antibody-ELISAs in order to identify herds where the parasite infection level is likely to cause production loss (F. hepatica and O. ostertagi) (defined as economic infections) or where patent infections have been present over the past grazing season (D. viviparus). The herd prevalence of economic infections with F. hepatica and O. ostertagi was 37.3% (95% Confidence Interval (CI): 35.1-39.7) and 59.1% (95%CI: 56.8-61.4), respectively. The herd prevalence of D. viviparus was 19.6% (95%CI: 17.7-21.6). On 28.9% (CI 26.8-31.3) of the herds, low levels of infection were observed for all three of the helminths. The presence of clustering of (economic) infections was studied using Morans I, whereas the location and size of the clusters were studied using the spatial scan statistic, the Local Indicator of Spatial Association and Kernel density plotting. A marked clustering in the spatial distribution of F. hepatica and a mild clustering in the spatial distribution of O. ostertagi were observed. D. viviparus infections were spread evenly over Flanders. Knowledge of locations of high risk areas can lead to increased awareness and may be the start of the development of regionally adapted control measures.

Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle.

Fasciola hepatica is a pathogenic trematode parasite of ruminants with a global distribution. Here, we briefly review the current epidemiology of bovine fasciolosis in Europe and discuss the progress made over the last decade in the diagnosis, impact on production and prediction of F. hepatica in cattle. Advances in diagnosis have led to significantly improved coprological and serological methods to detect presence of infection. Diagnostic test results have been correlated with intensity of infection and associated production losses, unravelling the impact on carcass weight and milk yield in modern cattle production systems. The economic impact of fasciolosis may, however, go beyond the direct impacts on production as evidence shows that F. hepatica can modulate the immune response to some co-infections. Control of bovine fasciolosis remains hampered by the limitations of the currently available flukicidal drugs: few drugs are available to treat dairy cows, many have low efficacies against juvenile stages of F. hepatica and there is evidence for the development of drug resistance. This makes research into the prediction of risk periods, and thus the optimum application of available drugs more pertinent. In this field, the recent research focus has been on understanding spatial risk and delivering region-specific spatial distribution maps. Further advances in epidemiological and economic research on bovine fasciolosis are expected to deliver farm-specific economic assessments of disease impact, to leverage non-chemotherapeutic management options and to enhance a more targeted use of anthelmintics.

Epidemiology and risk factors for exposure to gastrointestinal nematodes in dairy herds in northwestern Europe

In this survey, the epidemiology of gastrointestinal (GI) nematodes in dairy herds in five northwestern European countries was studied using a standardized Ostertagia ostertagi ELISA applied on bulk-tank milk, and a common questionnaire. The levels of exposure to GI nematodes were high in Belgium, the UK and Ireland, intermediate in Germany and low in Sweden, with a mean (95% confidence interval) ELISA result (ODR) of 0.83 (0.82-0.84) in Belgium, 0.82 (0.79-0.84) in the UK and 0.80 (0.78-0.83) in Ireland; significantly higher than the mean ODR of 0.66 (0.65-0.68) in Germany and 0.52 (0.51-0.53) in Sweden. Taking into account previous literature, these regional differences are likely to be systematic. Regional variations in exposure were significantly explained by differences in management (grazing time per day, mowing, the months of turnout, housing and anthelmintic treatment). However, after controlling for these factors, significant regional differences in levels of exposure remained, suggesting an importance for climate (temperature, rainfall) and unmeasured management factors. This study emphasizes that GI nematode-induced production losses should be considered on a large percentage of northwest European dairy herds. Proposals are made for the development of region-specific monitoring and control strategies. Further advances in this area are likely to come from intervention studies that investigate the feasibility of control measures and from studies on the potential effects of climatic conditions on shifts in levels of exposure between years and regions.

Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments

Due to the development of anthelmintic resistance, there have been calls for more sustainable nematode control practices. Two important concepts were introduced to study and promote the sustainable use of anthelmintics: targeted treatments (TT), where the whole flock/herd is treated based on knowledge of the risk, or parameters that quantify the severity of infection; and targeted selective treatments (TST), where only individual animals within the grazing group are treated. The aim of the TT and TST approaches is to effectively control nematode-induced production impacts while preserving anthelmintic efficacy by maintaining a pool of untreated parasites in refugia. Here, we provide an overview of recent studies that assess the use of TT/TST against gastrointestinal nematodes in ruminants and investigate the economic consequences, feasibility and knowledge gaps associated with TST. We conclude that TT/TST approaches are ready to be used and provide practical benefits today. However, a major shift in mentality will be required to make these approaches common practice in parasite control.

The bias, accuracy and precision of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods

The faecal egg count reduction test (FECRT) is the recommended method to monitor anthelmintic drug efficacy in cattle. There is a large variation in faecal egg count (FEC) methods applied to determine FECRT. However, it remains unclear whether FEC methods with an equal analytic sensitivity, but with different methodologies, result in equal FECRT results. We therefore, compared the bias, accuracy and precision of FECRT results for Cornell-Wisconsin (analytic sensitivity = 1 egg per gram faeces (EPG)), FLOTAC (analytic sensitivity = 1 EPG) and McMaster method (analytic sensitivity = 10 EPG) across four levels of egg excretion (1-49 EPG; 50-149 EPG; 150-299 EPG; 300-600 EPG). Finally, we assessed the sensitivity of the FEC methods to detect a truly reduced efficacy. To this end, two different criteria were used to define reduced efficacy based on FECR, including those described in the WAAVP guidelines (FECRT <95% and lower limit of 95%CI <90%) (Coles et al., 1992) and those proposed by El-Abdellati et al. (2010) (upper limit of 95%CI <95%). There was no significant difference in bias and accuracy of FECRT results across the three methods. FLOTAC provided the most precise FECRT results. Cornell-Wisconsin and McMaster gave similar imprecise results. FECRT were significantly underestimated when baseline FEC were low and drugs were more efficacious. For all FEC methods, precision and accuracy of the FECRT improved as egg excretion increased, this effect was greatest for McMaster and least for Cornell-Wisconsin. The sensitivity of the three methods to detect a truly reduced efficacy was high (>90%). Yet, the sensitivity of McMaster and Cornell-Wisconsin may drop when drugs only show sub-optimal efficacy. Overall, the study indicates that the precision of FECRT is affected by the methodology of FEC, and that the level of egg excretion should be considered in the final interpretation of the FECRT. However, more comprehensive studies are required to provide more insights into the complex interplay of factors inherent to study design (sample size and FEC method) and host-parasite interactions (level of egg excretion and aggregation across the host population).

A survey of the exposure to Ostertagia ostertagi in dairy cow herds in Europe through the measurement of antibodies in milk samples from the bulk tank

Measurement of antibodies to Ostertagia ostertagi in bulk tank milk (BTM) has value as a diagnostic indicator for potential production losses and anthelmintic treatment responses in dairy herds. Most of the recent data on O. ostertagi antibodies in milk have been generated in Belgium and Canada; the purpose of this study was to determine the range of O. ostertagi antibody levels in several European countries. BTM samples were collected during the autumn of 2005 and 2006 from a total of 1185 dairy herds from dairy farming regions in Denmark, Germany, Ireland, Italy, the Netherlands, Portugal, Spain and the United Kingdom. Antibody titres to O. ostertagi were determined by indirect ELISA and expressed as optical density ratios (ODR). In addition, relationships between ODR and management practices were investigated. For each country the mean ODR and the 25th-75th percentile values were determined. Mean BTM ODR values in herds with access to yards, paddocks and pastures ranged from 0.3 in Italy to 0.6 in Portugal and the UK/Ireland. The BTM ODR values obtained in this study were generally lower than those described in the literature for Belgium, but comparable with those in Canada. Variations between different European countries appeared to reflect different husbandry practices, particularly those related to access to pasture. The association analyses showed correlations between the BTM O. ostertagi ODR, outside access and grazing management, consistent with the publications from Belgium and Canada. When diagnostic values appropriate for different production situations and environments have been further validated, the test will provide an objective, quantitative assessment of the O. ostertagi status of a dairy herd and the possible impact this may have on performance and potential responses to anthelmintic treatment. This represents a significant step forward in evidence-based medicine for dairy veterinarians, advisors and farmers.