The number of goat farms is growing globally due to the expanding demand for goat dairy products , and the CR is no exception. Goats are a species of livestock known for their sensitivity to parasitic infections. Monitoring and optimising practices of parasite control in this growing sector, including the rational use of anthelmintics to delay the emergence of resistance, is therefore timely. AR in goats has been well documented in several European countries, but data for the CR are lacking. Our survey provides a first assessment of the resistance of strongylid nematodes to anthelmintics in Czech goat herds.
We identified a high prevalence of BZ resistance, and IVM and multiple resistance were moderately prevalent. European nationwide surveys have found that resistance against BZs is already well established in goat herds in France [14, 15], Slovakia , and Denmark . BZ resistance is as widespread in these countries as in our survey, mostly due to the strong reliance on BZs, e.g. 97% of French goat farmers use BZs, with this anthelmintic class representing > 84% of annual treatments . Many farmers prefer these drugs because of their reasonable price and the short period of milk withdrawal. Resistance to MLs is much less pronounced in goats, likely because the vast majority of European goat farms are specialised in milk production and because the use of most MLs is limited to non-lactating animals. The prevalence of ML resistance in Switzerland is higher than the prevalence detected in our survey [17, 18] or in Denmark , probably associated with the preference for MLs. Eprinomectin in a pour-on formulation is especially popular in Switzerland due to the convenient route of administration and a zero period of milk withdrawal. A survey conducted by Murri et al.  found that 86% of Swiss farmers have used this drug in goats. Multiple AR at some European goat farms has been reported [20, 21], but the current spread of this phenomenon in European countries [33, 34] is alarming and consistent with our results.
The richness of nematode species resistant to BZs should only be evaluated using the EHT based on molecular identification of L1 larvae, but we did not focus on this aspect in our survey. The LDT in our survey identified multispecies resistance to IVMs; Teladorsagia/Trichostrongylus and Haemonchus were common at IVM-AG concentrations considered to indicate resistance. The species richness of IVM-resistant nematodes identified in this survey mirrored the nematode species identified recently in goats in the CR  and is consistent with the richness detected in some European goat herds resistant to MLs [20, 36]. Haemonchus is nevertheless a major nematode genus resistant to MLs at the majority of goat farms throughout Europe [17, 37, 38]. Multiple-resistant strains of this nematode have also been isolated from goats in several European countries [33, 34, 39]. Haemonchus is at a higher risk of ML resistance than other nematodes, emerging presumably due to the lower sensitivity of Haemonchus females to IVMs  and to the very high prolific potential  and high genetic diversity of this genus . If Czech farmers continue to practise the current measures of parasite control and if climate change continues as expected, then Haemonchus may remain a major resistant species in the near future in goat herds in the CR.
In addition to monitoring AR, understanding the risk factors promoting the development of AR is essential in every country. The detection of these factors is unfortunately difficult, because of the multifactorial basis of AR, and requires many observations. Only a few studies have thus identified the factors contributing to the development of AR. A systematic review and meta-analysis of risk factors for AR in sheep only identified the frequency of treatment as an important factor . Similar analyses have yet to be conducted for goats, but none of the putative risk factors in a survey of Swiss goat herds were associated with eprinomectin resistance . Only stocking rate and farming experience in our survey were significantly associated with AR.
Overcrowding is a common predisposition of many diseases, and intensities of GI nematode infections are high when animals are assembled at high stocking rates. AR may thus be expected at high population densities of animals on pasture. Gaba et al.  clearly demonstrated that the higher the stocking rate, the greater the selective pressure for AR. These results are consistent with our survey. We detected a higher proportion of resistance to both anthelmintic classes evaluated (including multiple resistance) when the stocking rate exceeded eight goats per hectare. This association, however, was only significant for resistance to IVM. The level of IVM resistance was five-fold higher and was present in multiple nematode species in herds with high stocking rates. Our results suggest that resistance to IVM is already well established in these goat herds and that farmers should avoid the use of IVM in the future. Drug persistence could account for the significant association between stocking rate and IVM resistance in our survey. IVM is more persistent than BZs, which can accelerate the development of resistant nematode populations [44, 45]. Nematodes entering the host during the elimination of a drug are exposed to doses lower than the therapeutic dose, and high population densities of animals on a pasture may exacerbate this problem. Stocking rate should thus be an important consideration in both parasite control and the delay of AR development. Establishing general recommendations for optimal stocking rates is challenging, and farmers should take several factors into account (e.g. weight of animals, type of animal breeding, pasture size and composition, and current meteorological conditions). The frequency of resistant alleles will increase substantially at a stocking rate of 16 sheep per hectare and very high levels of AR may be expected at a stocking rate of 20 sheep . Similar studies for goats have yet to be conducted, but stocking rates lower than those published for sheep may be recommended for goats due to the ability of goats to shed higher numbers of nematode eggs compared to sheep.
Many farmers in the CR (especially the young ones) have begun to raise goats in the last decade. Establishing a commercial farm requires specific knowledge and experience, which is a challenge for new farmers . Acquiring sufficient practical experience in farming generally requires several years, and poor pasture and management of nutrition and health within this period may cause severe health problems in a herd. Inexperienced farmers generally consider parasites as the sole source of these problems and rely strongly on anthelmintics, so other measures to improve health (e.g. feed supplements) are not practised. Farmers frequently drench their animals when health and body conditions do not improve. Our survey identified BZ resistance at all goat farms where farmers had less than five years of experience. The relationship between these factors may be due to the preference of new farmers to use BZs instead of other drug classes. A reasonable price, a short period of milk withdrawal, and the predominant peroral formulation make BZs their drugs of choice. All low experienced farmers in our survey used these drugs almost exclusively. The probability of developing AR decreases when farmers accumulate knowledge and practical experience over time. The prevalence of BZ resistance in our study was 1.4-fold lower at farms led by experienced farmers. Similar trends were observed for IVM resistance but were not significant.
Other factors evaluated in our survey (including targeted selected treatment [TST] or underdosing) were not significantly associated with AR. TST is a promising strategy to effectively control nematode infections while maintaining anthelmintic efficacy [47, 48]. Anthelmintic treatment based on this approach is administered only to animals that are obviously suffering from nematode infections, and such treatment is beneficial to them because it enhances both their health and production [49, 50]. Our survey found evidence of BZ resistance at all farms where TST was practised and of IVM resistance at half of the farms and detected multiple resistance. The choice of treatment indicator, however, is crucial for the efficacy of TST [51, 52]. Czech farmers traditionally select animals for drenching based on faecal consistency (diarrhoea), but this indicator is unreliable for TST in goats .
A more rapid metabolism of xenobiotics is responsible for the faster clearance of anthelmintics from goats than sheep. Drenching goats at the standard dose recommended by the manufacturer (sheep dose) will thus lead to underdosing [8, 54]. Insufficient doses of a drug permanently administered to goats is one of the most important factors responsible for the high prevalence of AR in this livestock species [9, 55, 56]. Goats should be treated at about 1.5 times the recommended sheep dose rates for MLs and at twice the recommended sheep dose rates for BZs to achieve the same therapeutic effect as in sheep . Very high prevalences of resistance, including multiple resistance, were detected at farms where standard sheep doses had been used for many years [14, 15, 20], but this factor was not significantly associated with AR in our survey.