Anthelmintic resistance in gastrointestinal Strongylidae in sheep and goats: new data on prevalence, epidemiology, preventive measures and alternatives to anthelmintic drugs

Anthelmintic-resistant gastrointestinal nematodes represent the major problem in controlling of parasites of small ruminants in central Europe. This article gives a brief update on the prevalence of resistant populations in sheep and goat farms in Europe. New data on the selection and spread of anthelmintic resistance are reported and recommendations are given for minimising further increases in the incidence of resistant populations. New strategies which may play a role in integrated control programs in the future, e.g. vaccination and the development of nematode-resistant breeds of animals or of nematophagous fungi are briefly discussed.     

Endoparasite control.

The gastrointestinal nematodes are considered to be the most important group of internal parasites. Gastrointestinal parasitism is a major constraint to animal health, productivity, and profitability in grazing livestock production systems. The clinical manifestations of infection may range from no apparent effect to death. Despite years of research, assessment of production losses in many regions of the United States and of the potential impact of gastrointestinal nematode control remains to be determined.     

Anthelmintics for cattle

A number of anthelmintics are available for the control of gastrointestinal nematodes in cattle. In North America, O. ostertagi, Cooperia spp., lung worm, and F. hepatica probably cause the greatest losses in production. The older anthelmintics are often deficient in their action against some of these parasites. Recently, the Paratect morantel tartrate slow-release bolus has provided a mechanism for the prevention of infections with gastrointestinal nematodes and lung worm, to some extent, and this has been shown to produce considerable economic benefits. Fenbendazole removes arrested O. ostertagi larvae; thus, its availability is an important step in the prevention of type-2 ostertagiasis. It also has a very broad spectrum of activity that includes most other nematodes and tapeworms and is a very safe anthelmintic. Ivermectin is highly effective against almost all cattle nematodes and also has great value for the control of arthropod ectoparasites. In addition, it and levamisole are the only anti-nematode drugs that can be administered to cattle by injection. Clorsulon is a new, safe anthelmintic that provides good control of liver fluke and, thus, fills a gap in the control of helminths of cattle in North America. The efficient use of anthelmintics in association with management based on a knowledge of parasite epidemiology can ensure that cattle do not rapidly become re-infected. In this way, the benefits from the use of anthelmintics can be very considerable and far greater than the costs of control.     

The comparative efficacy of abamectin, monepantel and an abamectin/derquantel combination against fourth-stage larvae of a macrocyclic lactone-resistant Teladorsagia spp. isolate infecting sheep

Anthelmintic resistance by gastrointestinal nematodes of sheep continues to be an issue of global interest. While the recent introduction in some countries of one or two new anthelmintic classes (amino-acetonitrile derivatives [AAD] and spiroindoles [SI]) has been welcomed, it is important that there is no relaxation in parasite control and the management of drug resistance. Monepantel (an AAD) was the first new anthelmintic to be approved for use (New Zealand, 2009) and was followed a year later in the same country by a combination of derquantel (a SI) and abamectin. The present study determined the efficacy of the new anthelmintic products and abamectin against fourth-stage larvae of macrocyclic lactone-resistant Teladorsagia spp. in lambs. Efficacies were calculated by comparing post-mortem nematode burdens of treated animals with those of untreated control sheep, and were 98.5, 86.3 and 34.0% for monepantel, abamectin/derquantel and abamectin, respectively. The nematode burdens of monepantel- and abamectin/derquantel-treated sheep were significantly lower than those sheep treated with abamectin and the untreated controls. Similarly, the burden of the monepantel group was significantly lower than that of the abamectin/derquantel group. These findings provide an opportunity to reinforce the recommendation that farmers and animal health advisors need to know the resistance status of nematode populations on subject farms to ensure effective control programs are designed and implemented. Such control programs should include an appropriate choice of anthelmintic(s), monitoring parasite burdens for correct timing of treatments, and pasture management to reduce larval challenge balanced with the maintenance of drug-susceptible populations in refugia.     

Anthelmintic resistance in sheep in Europe: A selected review

Intensive use of anthelmintics to control gastrointestinal nematodes selects for anthelmintic resistance, which has become an important issue in many European countries. Presence of nematode strains resistant to benzimidazoles, imidazothiazoles and/or macrocyclic lactones has been repeatedly reported, particularly for the three most important genera, Haemonchus, Teladorsagia and Trichostrongylus. Additionally, multiple drug-resistant populations of these parasites have also been detected. Examples are given for the situation in European countries with differing climatic conditions and management systems of small ruminants. The widespread emergence of multi-resistant nematodes proves that the past intensive suppressive chemical control strategies may not be a successful approach any longer. Experience from the up to now development of anthelmintic resistance suggests that modern control schemes should not rely on sole use of anthelmintics, but employ other, more complex and sustainable recipes, combing chemical, environmental and immunological control.     

Management and control of gastrointestinal nematodes in communal goat farms in Zimbabwe

Goats are an important source of livelihood especially in smallholder communities. Infections with gastrointestinal nematodes (GIN) remain the most prevalent parasitic diseases affecting small ruminants. The study was conducted to assess management, the level of knowledge and control of gastrointestinal nematodes. Surveys were conducted in Chipinge, Shurugwi, Binga, Tsholotsho and Matobo districts, representing the five natural/agro-ecological regions (NR) in Zimbabwe. Data was collected in 135 households using a pre-tested semi-structured questionnaire. Results indicated that goats were ranked the most important livestock species, with high flock sizes in NR IV and V. Partitioning of roles was such that the adult males were involved in decision-making while females and children were involved in day-to-day management of animals. Farmers showed low levels of input use, with natural pasture (98.4%) being the main feed source and indigenous breeds (73.2%) being kept. Farmers ranked food and financial benefits as the main reasons for keeping goats. Gastrointestinal nematodes ranked the highest as the most common disease, with majority of farmers (57%) not controlling or treating animals and 63% of farmers not having knowledge on the spread of GIN. Access to veterinary services, anthelmintic class used and breeds used by the farmers had the highest effects on parasitic infections in households. Farmer education is required for capacitation of farmer in terms of disease prevention and control so as to improve goat production.     

Integrated parasite management: products for adoption by the Australian sheep industry

The increasing cost of production loss caused by gastrointestinal nematodes (GIN) highlights the importance of good control programs. However, the endemic nature of anthelmintic resistance also reminds of the need for nonchemical options. Both chemical and nonchemical control options need to be integrated into regional parasite management programs (IPM) with the emphasis on component options determined by factors such as major GIN species, regional climate, property size and enterprise structure. The Integrated Parasite Management of Sheep project was established to develop and demonstrate regional parasite control programs, that integrated chemical and nonchemical options, for the main sheep-producing regions of Australia. The project included research about the ecology of the main endo and ecto-parasites of sheep and a national survey of parasite control practices by sheep producers. IPM approaches developed for two contrasting regions of Australia are discussed. Barriers for the adoption of IPM programs include perceived complexity associated with a multi-component approach, time requirements and difficulty. Facilitating the industry adoption of IPM programs is discussed with relevance to the use of small group extension and involvement of the commercial sector. Perceptions of complexity of IPM may be managed by facilitating adoption of components in a step-wise process such that learning outcomes accumulate over time. Extension efforts must address the needs of industry sectors other than sheep producers and explore user pay approaches. The success of these approaches will depend on the relation of the extra profit to producers, through adoption of IPM programs, with remuneration sufficient to attract a commercial service.     

Targeted selective treatment for worm management-How do we sell rational programs to farmers?

Seriously escalating global anthelmintic resistance in gastrointestinal nematodes of small ruminants has spawned a variety of alternatives to anthelmintics for worm management, based on the need for sustainable Integrated Parasite Management (sIPM). Pivotal to the sIPM approach is the concept of refugia, the proportion of a given parasite population that escapes exposure to control measures. By balancing drug applications with the maintenance of refugia, the accumulation of anthelmintic resistance alleles in worm populations can be considerably delayed, while still providing good levels of control. The over-dispersed nature of parasitic infections provides an opportunity to achieve this balance, by targeting treatments to the members of a flock or herd that are least tolerant to nematode infection. However, implementation of this strategy has only recently become feasible, with the development of the FAMACHA((c)) system for clinical evaluation of anaemia due to haemonchosis. Subsequently, the use of milk yields has proven an effective indicator in dairy goats infected predominantly with nematodes other than Haemonchus contortus. In addition, short-term weight changes and perhaps also body condition scoring may provide indices of parasitism, permitting the rapid identification of animals likely to benefit from treatment. However, sIPM and refugia-based approaches are more complex than whole-flock treatments in conventional programs, and adoption by farmers is most likely where the theoretical basis is understood. As close communication with informed advisors is generally limited, there is a danger that sIPM will remain a theoretical concept without alternative modes of communication. The development of computer-based decision support programs, which use epidemiological, seasonal and clinical information to provide recommendations for specific situations, should be accorded high priority in the future development of worm management systems.     

牛羊线虫抗药性及其PC检测技术研究进展

牛羊线虫病是严重影响牛羊生产性能和经济效益的主要寄生虫病，化学药物是目前防治本病的主要手段，近年来线虫抗药性。已经成为世界各地牛羊线虫控制中的首要问题。建立线虫抗药早期检测技术可以时了解抗药性及其产生的条件等，便于采取有效对策，本文简要阐述牛羊线虫抗药性的分布与检测，现有抗药性检测方法的缺点以及PCR检测技术的最新进展。     

Use of the sustained-release morantel bolus in stocker calves in southern United States

Two groups of 21 mixed-breed heifers were wintered on separate permanent pastures. Each heifer from one group was administered a sustained-release morantel bolus on October 7 (day 0), and the other group remained as untreated controls. Body weights were determined and fecal samples were taken at 28-day intervals. At the onset of the trail and at every 56 days, 6 heifers were removed from each group for slaughter to determine the developmental stages and the number of gastrointestinal nematodes. In addition, 3 tracer calves that were free of gastrointestinal nematodes were released on each pasture for 28 days at the beginning of the trail and after the last experimental-group calves had been removed. The 6 calves slaughtered on day 0 of the trail had a mean of 5,544 gastrointestinal nematodes. Tracer calves released on day 0 and removed on day 28 of the trial acquired 31,143 and 30,530 gastrointestinal nematodes from the pastures containing the treated and control heifers, respectively. Throughout the trial, the number of nematodes in the control calves increased at each sampling date (mean, 126,168 worms), whereas the mean number of worms in the treated heifers was 45,458. Tracer calves placed in the pastures after the 168-day trail acquired significantly more worms (9,632 vs 2,899; P less than 0.05) from grazing the pastures with control heifers than from grazing the pastures with treated heifers. Counts of eggs per gram of feces were significantly different (P less than 0.01) between the 2 groups from day 28 through day 112.(ABSTRACT TRUNCATED AT 250 WORDS)     

An abattoir survey of gastrointestinal nematode infections in cattle in the central highlands of Kenya

The gastrointestinal tracts of 672 crossbred cattle were obtained from various abattoirs in Kiambu District, Kenya from August 1992 to July 1993, and examined for the presence of gastrointestinal nematodes. Eight nematode species were found in 583 (86.8%) of the animals. The nematodes were, in order of prevalence: Haemonchus placei (67.0%), Cooperia pectinata (53.0%), Cooperia punctata (41.7%), Oesophagostomum radiatum (38.4%), Trichostrongylus axei (24.3%), Nematodirus helvetianus (19.6%), Trichuris globulosa (9.7%) and Strongyloides papillosus (3.6%). The intensity of the nematode infection was moderate; the mean burden being less than 7000 worms. H. placei accounted, on average, for 52.3% of the total burden. The total burden was least during the dry seasons and increased gradually during the rainy seasons. Adult H. placei persisted in the host throughout the year and there was no indication of hypobiosis. The heaviest gastrointestinal worm burdens were detected in 1.5- to 3-year-old animals. These findings are discussed with regard to their relevance for strategic control of gastrointestinal nematodes in cattle.     

Comparison of efficacy of selamectin, ivermectin and mebendazole for the control of gastrointestinal nematodes in rhesus macaques, China

An experiment was conducted to evaluate the efficacy of ivermectin and mebendazole compared with selamectin against gastrointestinal nematodes in rhesus macaques. A total of 60 rhesus macaques (Macaca mulatta), which were all infected with gastrointestinal nematodes, were randomly assigned to three treatment groups (selamectin, ivermectin and mebendazole) and one control group. Fecal samples for determining nematode egg counts were collected pre- and post-treatment. All treatments resulted in decrease in the number of eggs per gram (EPG) in the post-treatment sample compared with the pre-treatment sample. Reductions of mean egg counts from day -3 levels were 99.4% for selamectin, 99.2% for ivermectin and 99.4% for mebendazole on trial day 11, respectively. However, no significant difference was found among treatment groups. According to the data demonstrating a similar efficacy in selamectin-, ivermectin- and mebendazole-treated rhesus macaques, it was effective and convenient to apply either selamectin and ivermectin or mebendazole in rotation on the local conditions.     

Control of gastrointestinal parasitism with nematodes in dairy goats by treating the host category at risk

Infections of the gastrointestinal tract with parasitic nematodes remain one of the main limiting factors in grazing dairy goats. The usual mode of control of these parasitic diseases has up to now been based on the repeated use of anthelmintics. However, the prevalence rates of anthelmintic resistances, in particular to benzimidazoles, are now particularly high in the French dairy goat production. This situation makes it mandatory to reconsider the usual mode of control of these nematodes and to look for short term, alternative solutions which combine the control of gastrointestinal infections and management of anthelmintic resistances. One of the possible options is to leave a part of the flock without treatment during the grazing season in order to maintain alleles of susceptibility to anthelmintics within the worm populations. Previous epidemiological observations identifying the categories of host populations at risk are presented which provide the rationale for targeted applications of treatments. The results of assays on experimental flocks and from farm surveys examining the advantages and drawbacks of selective treatments are presented. The value of these results in combination with other alternative solutions of control are discussed in order to use minimum treatments with maximum benefits.     

Seasonal Prevalence of Gastrointestinal] nematodes of goats in Pernambuco state, Brazil

During each of 36 1-month periods from April 1979 to March 1982, 3–4 goats selected from typical farms were necropsied and examined for gastrointestinal nematodes. The goats were male, 12 months old, born on the farm and raised without any anthelmintic application. At the beginning of each month, from April 1981 to March 1982, three 12-month-old male goats shown to be free of gastrointestinal nematodes after anthelmintic treatment were grazedwith a flock of naturally infected goats (tracer goats). At the end of each month, these goats were placed on a cementfloored pen and were maintained there for 4 weeks prior to necropsy and examination for gastrointestinal nem nematodes.

Every goat examined was found to be parasitized by more than one species of nematode. Haemonchus contortus, Strongyloides papillosus and Oesophagostomum columbianum were the most prevalent nematodes found. Total worm burdens present in the farm animals were highest during late rainy/early dry season (March-June) and lowest in mid-rainy season (January-February). The acquisition of nematodes by tracer goats occurred mainly from mid-rainy to early dry season (January-June).     

Local inflammation as a possible mechanism of resistance to gastrointestinal nematodes in Angus heifers

Understanding mechanisms of resistance to gastrointestinal nematodes is important in developing effective and sustainable control programs. A resource population of Angus cattle consisting of approximately 600 animals with complete pedigree records has been developed. The majority of these animals were completely characterized for their resistance to natural challenge by gastrointestinal nematodes. As the first step towards understanding the molecular basis of disease resistance, we investigated expression profiles of 17 cytokines, cytokine receptors, and chemokines using real-time RT-PCR in animals demonstrating resistance or susceptibility to pasture challenge. The animals exposed to natural infection for approximately 6 months were treated to remove existing parasites and then experimentally challenged with both Ostertagia ostertagi and Cooperia oncophora. The mRNA expression profiles of these genes in abomasal and mesenteric lymph nodes (ALN, MLN), fundic and pyloric abomasa (FA, PA), and small intestine (SI) were compared between resistant and susceptible animals. Resistant heifers exhibited elevated expression of inflammatory cytokines such as TNFalpha, IL-1beta, and MIP-1alpha in fundic and pyloric abomasa 7 days post infection. Expression levels of IL-10, polymeric immunoglobullin receptor gene (PIGR), and WSX-1 were also 2.7-19.9-folds higher in resistant than susceptible heifers in these tissues. No difference in expression of CXCL6, CXCL10, IFN-gamma, IL-2, IL-4, IL-6, IL-8, IL-12 p40, IL-13, IL-15 and IL-18 was observed between the two groups. The expression of MIP-1alpha, IL-6, and IL-10 was also elevated in small intestines in resistant animals. In contrast, little difference in expression of these genes was detected between resistant and susceptible groups in the draining lymph nodes. These data indicate that resistant animals can better maintain inflammatory responses at the site of infection, suggesting a possible novel mechanism of resistance.     

Opossum Nematodiasis: Diagnosis and Treatment of Stomach,Intestine, and Lung Nematodes in the Virginia Opossum (Didelphis virginiana)

Internal parasitic infections are common in the Virginia opossum (Didelphis virginiana). More than 50 different species of nematodes have been identified from the genus Didelphis. Of them, 3 can cause significant illness to native opossums in Southern California, 2 gastrointestinal nematodes and 1 pulmonary nematode. This article provides an overview of the life cycles, methods for identification, pathologic findings, diagnostic tests, clinical signs, and options for treating these common nematode species.     

Eradication of targeted species of internal parasites

Eradication can be defined as the permanent reduction to zero of the incidence of infection caused by a specific agent as a result of deliberate efforts. Eradication strategies must be designed to increase access to and utilization of veterinary and animal health support services beyond that normally achieved by routine services. Consequently, before undertaking an eradication program, proponents must be certain that they can be sure of a commitment of resources sufficient to complete the project. A helminth eradication campaign would require the application of anthelmintics to all hosts at a level aimed at killing heterozygote resistant individuals. This strategy runs counter to the prevailing opinion that resistance to chemicals will always occur and control schemes should accept some production loss by letting a proportion of parasites escape selection (in refugia) and thereby increase the useful life of the chemical. Under certain circumstances, environmental constraints may make some species of parasitic nematodes vulnerable to an eradication program. Anthelmintics have been used to exploit these constraints in past control programs and have lead to local eradication of several species of gastro-intestinal parasitic nematodes. Also, there are at present eradication programs for nematode parasites of human that are based on anthelmintic treatment. However, the suppressive pesticide treatment required to bring about the virtual elimination of species is a high-risk strategy and should only be undertaken if eradication is an achievable goal. It is also important to plan an exit strategy if eradication fails.     

Efficacy of the morantel sustained release trilaminate matrix against gastrointestinal nematodes in beef calves

The effectiveness of the morantel sustained release trilaminate (MSRT) in controlling gastrointestinal nematodes through a grazing season was evaluated using 60 yearling beef stocker calves randomly divided into 2 groups of 30 animals each. In April 1985, the calves comprising the treatment group each received an MSRT designed to release morantel tartrate continuously for 90 days while those of the control group remained unmedicated. All animals were weighed and samples of rectal feces were taken at 14-day intervals, beginning on Day 0, until trial termination (Day 168). At trial termination, 10 control and 10 treated calves were necropsied for recovery of gastrointestinal nematodes. Three sets of parasite-na?ve tracer calves were utilized to evaluate the initial, interim and final levels of pasture contamination by nematode larvae. Overall, the use of the MSRT resulted in a 75.5% reduction (P less than 0.001) in output of nematode eggs from the principals, an 81.8% reduction (P less than 0.001) in numbers of gastrointestinal nematodes in principals (at trial termination), and a 96.9% reduction (P less than 0.05) of pasture larval nematode contamination (as indirectly indicated by parasite burdens in tracer calves). The mean weight advantage of treated calves was 16.6 kg per head (P less than 0.001).     

不同驱虫药物对奶山羊消化道线虫驱虫效果研究

本研究旨在观察不同驱虫药物对奶山羊消化道线虫的驱虫效果,为今后寄生虫病的防治筛选更好的驱虫药物。选取奶山羊96只,分3组,每组32只,分别投喂伊维菌素注射液、芬苯达唑粉和伊维菌素芬苯达唑预混剂3种驱虫药物,采用饱和盐水漂浮法和麦克马斯特法检测驱虫前后线虫的感染情况。结果发现:伊维菌素注射液组虫卵转阴率为6.25%;芬苯达唑粉剂组虫卵转阴率为31.25%;伊维菌素芬苯达唑预混剂组虫卵转阴率为50.00%。驱虫前后感染强度伊维菌素注射液组差异显著(P<0.05),芬苯达唑粉剂组差异极显著(P<0.01),伊维菌素芬苯达唑预混剂组差异极显著(P<0.01)。因此,建议采用伊维菌素芬苯达唑预混剂作为奶山羊消化道线虫首选驱虫药物。     

Genetic parameter estimates for gastrointestinal nematode parasite resistance and maternal efficiency indicator traits in Santa Inês breed

Infection with Haemonchus contortus is the most economically important gastrointestinal nematode parasitosis and the most important cause of mortality in sheep production. The aim of this study was to estimate variance components of gastrointestinal parasite resistance traits, maternal efficiency (ME) and ewe adult weight (AW) in Santa Inês breed in tropical conditions. The phenotypic records were collected from 700 animals, belonging to four flocks located south‐east and north‐east in Brazil. The evaluated traits were as follows: degree of anaemia assessed using the FAMACHA chart (FMC), haematocrit (HCT), white blood cell (WBC), red blood cell (RBC), haemoglobin (HGB), platelets (PLT), faecal egg count (EPG_log), ME, metabolic maternal efficiency (MME), AW and metabolic ewe adult weight (MAW). From the 700 animals, 576 (82% of the evaluated population) were genotyped with the Ovine SNP12k BeadChip (Illumina, Inc.). Markers with unknown genomic position, located on sex chromosomes, monomorphic, with minor allele frequency <0.05, call rate <90% and with excess heterozygosity were excluded. The variance components were estimated using a single‐trait animal model with ssGBLUP procedure. The correlation between the parasite's resistance indicators and the ME suggested that selecting animals with both higher adult weight and ME will also favour the selection of animals with better resistance to gastrointestinal nematodes parasites, specially H. contortus. Therefore, since there are few or no studies with Santa Inês breed in this area, it is important to study those traits to better manage selection programs.