100 Questions in Livestock Helminthology Research

doi:10.1016/j.pt.2018.10.006

Trends in Parasitology

Volume 35, Issue 1, January 2019, Pages 52-71

https://doi.org/10.1016/j.pt.2018.10.006 Get rights and content

Highlights

Important questions on helminths of livestock were elicited across the research community and prioritised by online vote.

The approach contrasts with traditional review formats and seeks to identify questions agreed to be both important and feasibly addressed by focused research projects.

A shortlist of 100 questions is presented with supporting text to provide perspective.

The article is intended to stimulate new and ongoing research on helminth infections, in support of sustainable global livestock health and productivity.

An elicitation exercise was conducted to collect and identify pressing questions concerning the study of helminths in livestock, to help guide research priorities. Questions were invited from the research community in an inclusive way. Of 385 questions submitted, 100 were chosen by online vote, with priority given to open questions in important areas that are specific enough to permit investigation within a focused project or programme of research. The final list of questions was divided into ten themes. We present the questions and set them briefly in the context of the current state of knowledge. Although subjective, the results provide a snapshot of current concerns and perceived priorities in the field of livestock helminthology, and we hope that they will stimulate ongoing or new research efforts.

Section snippets

Towards Inclusive Identification of Research Priorities

The study of the helminth parasites of livestock is facing a period of rapid change. The availability of a series of highly effective and affordable anthelmintics (see Glossary) from the 1960s onwards coincided with the intensification of animal production systems in many parts of the world. As a result, adequate control of helminths could be achieved on the majority of farms with existing scientific knowledge, reducing incentives for investment in further research [1]. Currently, however, the

Hypobiosis

1. What determines emergence of arrested helminth stages in the host, for example, termination of hypobiosis in gastrointestinal nematodes in ruminants or cyathostomins in horses, or the end of the mucosal phase of ascarids in poultry?

Hypobiosis is important for perpetuation of helminth populations during adverse environmental conditions. While factors inducing hypobiosis are well described (e.g., cold or dry seasonal cues, or immunity), factors governing the period of inhibition and timing of

Section II. Economic and Environmental Impacts

12. What is the true financial cost of helminth infection?

13. Is profitable livestock husbandry possible without chemical parasite control?

14. Does the control of helminths reduce net methane emission over the lifetime of a ruminant?

15. How can environmental impacts of anthelmintics be properly measured, including on nontarget fauna, and ecosystem functioning and service provision?

16. What are the costs (financial, human, and to animal welfare) of anthelmintic resistance?

Section III. Effects on Host Behaviour and Welfare

17. How can we measure the impact of helminth infections on livestock welfare?

18. How does parasitism affect animal behaviour?

19. Can we use changes in behaviour to identify those individuals that need treatment?

20. Can we select for host behaviour to control helminths?

21. Do ruminants self-medicate by selectively grazing plants with anthelmintic compounds?

22. Are animals better off and healthier with some worms, rather than none? Studies are biased towards negative effects on hosts, and

Section IV. Host–Helminth–Microbiome Interactions

23. How do gastrointestinal parasites communicate in the gut?

24. How does interaction between different helminths in coinfection affect the immune system of the host and the development of disease?

25. Are there associations between animals’ microbiomes and helminth communities, and do they matter?

26. Can the alteration of gut microbiota influence immunity to parasites in livestock, and vice versa?

27. To what extent do coinfections between helminths and other specific pathogens – for example,

Section V. Host Resistance, Resilience, and Selective Breeding

28. Have 60 years of intense anthelmintic use changed the relative susceptibility of livestock to parasites? In other words, are animals less robust than they used to be as a result of protection from the effects of parasites by drugs, thereby causing selection of higher-producing but more parasite-susceptible animals?

29. How can host resilience and host resistance of ruminants to helminths be measured and distinguished?

30. Is resistance, tolerance, or resilience the best breeding objective to

Section VI. Development and Detection of Anthelmintic Resistance

38. What is the relative importance of management versus environmental factors in determining the development of anthelmintic resistance in livestock?

39. How does animal movement affect the spread of helminth infections and anthelmintic resistance?

40. What changes in genes other than those encoding the immediate drug target, such as transporters and drug metabolism, are involved in anthelmintic resistance?

41. What do we understand about the fitness costs of anthelmintic resistance, and how can

When to Intervene against Resistance

54. What is the usefulness of anthelmintics working at decreased (e.g., 50% or 80%) efficacy?

55. When should drug combinations be used to combat anthelmintic resistance, and when not?

Optimal usage of anthelmintic drugs in the face of AR should be tailor-made and consider parasite species, host species, farm management, and climatic factors 2, 3. Deciding how to extend the lifetime of drugs, either before or after some resistance is evident 64, 65, requires consideration of actual levels of AR

Section VIII. Vaccines and Immunology

72. Can the natural immune response to helminths be enhanced by applying a biological treatment (e.g,. specific cytokine or cytokine inhibitor) and thereby control infections?

73. Do worms have a microbiome? Can it be exploited as a vaccine or treatment target?

74. How can vaccines against helminth infections in ruminants be integrated in control programmes?

75. In what ways do helminths resist or escape from the host immune system?

76. How well do antihelminth vaccines have to work to be useful?

Plant-based Control

82. Many studies have shown a maximum efficacy of bioactive plant compounds around 60–70% reduction in gastrointestinal nematode burden: how can efficacy be driven higher? Is it needed?

83. Can different bioactive plants be combined to increase effects on gastrointestinal nematodes?

84. Can plants be cultivated for grazing that have maximum nutritive value and the potential to lower helminth burden?

85. How does processing and conservation of bioactive forages affect their efficacy?

86. What are

New Decision Support Tools for Helminth Control

92. How can different novel control methods for helminths be integrated effectively and in a way that is simple enough for farmers to implement?

93. Can helminth-control-decision-support tools be integrated effectively in farm or pasture management software?

94. How can we transfer automated technology to farmers, especially those who are resource-poor?

95. Is research in veterinary helminth infections reaching livestock farmers in developing countries and, if so, what is the impact?

Veterinary

Concluding Remarks

The questions listed above were the result of an attempt to elicit research priorities from a wider constituency than in more usual review formats, which are typically led by a small number of established experts. It was anticipated that this would yield a wider-ranging set of potential research topics and directions, less constrained by forces that shape disciplinary academic consensus. In the event, the topics and questions are broadly similar to those raised in recent expert reviews 1, 4, 6,

Acknowledgments

We thank the officers and members of the Livestock Helminth Research Alliance (LiHRA) for encouraging this initiative and giving space to it in their annual meetings, to the World Association for the Advancement of Veterinary Parasitology for permitting elicitation of questions as part of their 26th biennial conference in Kuala Lumpur, Malaysia, and to the editors of Trends in Parasitology for commissioning this article. The authors credit the EU for funding leading to this work through FP7

Glossary

Animal Task Force (ATF)Appendix A^vi: a European public–private platform that fosters knowledge development and innovation for a sustainable and competitive livestock sector in Europe (Box 1).
Anthelmintic: a chemical which can be used to control worm infections. Six different broad-spectrum classes are currently widely available for use in sheep (benzimidazoles, imidazothiazoles, tetrahydropyrimidines, macrocyclic lactones, amino acetonitrile derivatives, and spiroindoles) and four for cattle

References (104)

R.M. Kaplan et al.
An inconvenient truth: global worming and anthelmintic resistance
Vet. Parasitol.
(2012)
N.C. Sangster
Ten events that defined anthelmintic resistance research
Trends Parasitol.
(2018)
J.A. van Wyk
Blueprint for an automated specific decision support system for countering anthelmintic resistance in Haemonchus spp. at farm level
Vet. Parasitol.
(2011)
H.C. Gibbs
Hypobiosis in parasitic nematodes – an update
Adv. Parasitol.
(1986)
C. Cantacessi
Deep insights into Dictyocaulus viviparus transcriptomes provides unique prospects for new drug targets and disease intervention
Biotechnol. Adv.
(2011)
A. Rowe
Haemonchus contortus infection in sheep: Parasite fecundity correlates with worm size and host lymphocyte counts
Vet. Parasitol.
(2008)
J.G. Walker et al.
Generalists at the interface: Nematode transition between wild and domestic ungulates
Int. J. Parasitol. Parasites Wildl.
(2014)
K. Huson
Paramphistomosis of ruminants: an emerging parasitic disease in Europe
Trends Parasitol.
(2017)
M. Molento
Pasture larval count as a supporting method for parasite epidemiology, population dynamic and control in ruminants
Livest. Sci.
(2016)
J. Charlier
ECONOHEALTH: placing helminth infections of livestock in an economic and social context
Vet. Parasitol.
(2015)

A.R. Williams

A systems-life cycle assessment approach to modelling the impact of improvements in cattle health on greenhouse gas emissions

Adv. Anim. Biosci.

(2015)

A.S. Cooke

Modelling the impact of targeted anthelmintic treatment of cattle on dung fauna

Environ. Toxicol. Pharmacol.

(2017)

J.R. Verdu

Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: An interdisciplinary field study

Sci. Total Environ.

(2018)

B.D. Perry et al.

Improving the assessment of the economic impact of parasitic diseases and of their control in production animals

Vet. Parasitol.

(1999)

A.B. Forbes

Evaluation of the effects of nematode parasitism on grazing behaviour, herbage intake and growth in young grazing cattle

Vet. Parasitol.

(2000)

O. Szyszka

Do the changes in the behaviours of cattle during parasitism with Ostertagia ostertagi have a potential diagnostic value?

Vet. Parasitol.

(2013)

H. Hoste

Goat-nematode interactions: think differently

Trends Parasitol.

(2010)

W.C. Gause et al.

Macrobiota-helminths as active participants and partners of the microbiota in host intestinal homeostasis

Curr. Opin. Microbiol.

(2016)

L.E. Peachey

This gut ain’t big enough for the both of us. Or is it? Helminth–microbiota interactions in veterinary species

Trends Parasitol.

(2017)

N.R. Steenhard

Ascaris suum infection negatively affects the response to a Mycoplasma hyopneumoniae vaccination and subsequent challenge in pigs

Vaccine

(2009)

A. Andreasen

Immune and inflammatory responses in pigs infected with Trichuris suis and Oesophagostomum dentatum

Vet. Parasitol.

(2015)

L.E. Peachey

The relationships between faecal egg counts and gut microbial composition in UK thoroughbreds infected by cyathostomins

Int. J. Parasitol.

(2018)

A.W. Greer

Immune development and performance characteristics of Romney sheep selected for either resistance or resilience to gastrointestinal nematodes

Vet. Parasitol.

(2018)

D.G. Riley et al.

Genetic parameters for FAMACHA (c) score and related traits for host resistance/resilience and production at differing severities of worm challenge in a Merino flock in South Africa

Vet. Parasitol.

(2009)

A.J. Wolstenholme

Drug resistance in veterinary helminths

Trends Parasitol.

(2004)

F. Knapp-Lawitzke

Rapid selection for β-tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture

Vet. Parasitol.

(2015)

L. Rinaldi

Comparison of individual and pooled faecal samples in sheep for the assessment of gastrointestinal strongyle infection intensity and anthelmintic drug efficacy using McMaster and Mini-FLOTAC

Vet. Parasitol.

(2014)

F. Kenyon

Pooling sheep faecal samples for the assessment of anthelmintic drug efficacy using McMaster and Mini-FLOTAC in gastrointestinal strongyle and Nematodirus infection

Vet. Parasitol.

(2016)

M. George

Utilization of composite fecal samples for detection of anthelmintic resistance in gastrointestinal nematodes of cattle

Vet. Parasitol.

(2017)

J.A. van Wyk

Quality control in generic anthelmintics: Is it adequate?

Vet. Parasitol.

(1997)

J. Learmount

A computer simulation study to evaluate resistance development with a derquantel–abamectin combination on UK sheep farms

Vet. Parasitol.

(2012)

D.M. Leathwick

Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes

Int. J. Parasitol. Drugs Drug Resist.

(2015)

F. Kenyon

The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants

Vet. Parasitol.

(2009)

M.P. Cornelius

Computer modelling of anthelmintic resistance and worm control outcomes for refugia-based nematode control strategies in Merino ewes in Western Australia

Vet. Parasitol.

(2016)

F. Kenyon

A comparative study of the effects of four treatment regimes on ivermectin efficacy, body weight and pasture contamination in lambs naturally infected with gastrointestinal nematodes in Scotland

Int. J. Parasitol. Drugs Drug Res.

(2013)

J. Vlaminck

Vaccination of calves against Cooperia oncophora with a double-domain activation-associated secreted protein reduces parasite egg output and pasture contamination

Int. J. Parasitol.

(2015)

H. Rose

GLOWORM-FL: A simulation model of the effects of climate and climate change on the free-living stages of gastro-intestinal nematode parasites of ruminants

Ecol. Model.

(2015)

C.W. Sauermann et al.

A climate-driven model for the dynamics of the free-living stages of Cooperia oncophora

Vet. Parasitol.

(2018)

S.H. Verschave

Cattle and nematodes under global change: transmission models as an ally

Trends Parasitol.

(2016)

H. Hoste

Tannin containing legumes as a model for nutraceuticals against digestive parasites in livestock

Vet. Parasitol.

(2015)

H.M. Ropiak

Condensed tannins in extracts from European medicinal plants and herbal products

J. Pharm. Biomed. Anal.

(2016)

H. Hoste

Direct and indirect effects of bioactive legume forages against parasitic infections: experiences with tropical and temperate forages

Vet. Parasitol.

(2012)

A.R. Williams

Dietary cinnamaldehyde enhances acquisition of specific antibodies following helminth infection in pigs

Vet. Immunol. Immunopathol.

(2017)

E. Gaudin

Efficacy of sainfoin (Onobrychis viciifolia) pellet against multi resistant H. contortus and interaction with oral ivermectin: implication for on-farm control

Vet. Parasitol.

(2016)

J.M. Howell

Control of gastrointestinal parasite larvae of ruminant using nitrogen fertilizer, limestone and sodium hypochlorite solutions

Small Rumin. Res.

(1999)

C.L. Marley

The effect of dietary forage on the development and survival of helminth parasites in ovine faeces

Vet. Parasitol.

(2003)

W.F. Da Silveira

Nematophagous fungi combinations reduce free-living stages of sheep gastrointestinal nematodes in the field

J. Invert. Pathol.

(2017)

R.G. Woodgate et al.

WormKill to WormBoss: can we sell sustainable sheep worm control?

Vet. Parasitol.

(2012)

J. Learmount

Resistance delaying strategies on UK sheep farms: A cost benefit analysis

Vet. Parasitol.

(2018)

F. Vande Velde

Diagnosis before treatment: Identifying dairy farmers’ determinants for the adoption of sustainable practices in gastrointestinal nematode control

Vet. Parasitol.

(2015)

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A SURVEY OF ANTHELMINTIC EFFICACY IN DAIRY GOAT FARMS IN SOUTH-EAST FRANCE
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Goat’s milk production is an important activity in France. Gastrointestinal nematodes (GIN) remain a main threat for grazing goats, usually controlled using anthelmintic drugs (AH). However, 1) eprinomectin (EPN) is the sole molecule yet available without withdrawal time for milk in France; 2) nematodes AH resistances increase dramatically. First, a survey was performed on 13 farms in the Auvergne-Rhône-Alpes (AURA) region to evaluate the efficacy of 2 AH authorized for dairy goats: a benzimidazole (BZ) and a macrocyclic lactone (EPN pour-on). Fecal Egg Count Reduction Tests (FECRT) were carried out using 3 groups of 10 goats per farm: a control group, one treated with BZ (oxfendazole) and one treated with EPN. The results indicate a resistance to BZ in 11 out of 13 farms (84.6%) and a lack of efficacy for EPN pour-on in at least 10 farms (76.9%). Secondly, EPN was given orally or subcutaneously in 4 farms of the previous trial showing a lack of efficacy to EPN pour-on. A resistance to EPN was confirmed in 3 out of 4 farms. Although based on a few farms, these results confirm the high prevalence of resistance of GIN to BZ in dairy goat farms. They also highlight a high level of resistance to EPN and the lack of efficacy of EPN when used pour-on. Given the level of resistance to marketed drugs, there is an urgent need to explore alternative options to AH to prepare integrated, sustainable control of GIN.
Antagonism between co-infecting gastrointestinal nematodes: A meta-analysis of experimental infections in Sheep
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Gastrointestinal nematodes (GIN) have enormous global impacts in humans, wildlife and grazing livestock. Within grazing livestock, sheep are of particular global importance and the economics and sustainability of sheep production are greatly constrained by GIN infections. Natural infections are composed of co-infections with multiple species, and while some past work suggests species can interact negatively with one another within the same host, there is wide variation in reported patterns. Here, we undertook a systematic literature search and meta-analysis of experimental GIN co-infections of sheep to determine whether these experimental studies support the hypothesis of antagonistic interactions between different co-infecting GIN, and test whether aspects of parasite biology or experimental design influence the observed effects. A systematic search of the literature yielded 4848 studies, within which, we identified 19 experimental sheep studies comparing post-mortem worm counts across two co-infecting GIN species. Meta-analysis of 67 effects obtained from these studies provides strong evidence for interactions between GIN species. There was wide variation in the strength and direction of these interactions, but the global effect was significantly antagonistic. On average, there was a decrease in the number of worms of one species when a co-infecting species was also present, relative to a mono-infection with that species alone. This effect was dependent on the infectious dose and was rapidly lost after anthelmintic treatment, suggesting that live worms are required for the effect to occur. Individual parasite species varied in the extent to which they both exerted, and were subject to, these interspecies interactions, and these differences are more complex than simply co-localisation within the gastrointestinal tract. Antagonistic interactions between co-infecting GIN may feedback into their epidemiology as well as potentially affecting the clinical impacts of infection. Furthermore, the consequences of these interactions may be heightened when clinical interventions affect only one species within the co-infecting network. Whilst it was not possible to identify the causes of variation between GIN species in the impact of co-infection, these findings point to new avenues for epidemiological, clinical and mechanistic research on GIN co-infections.
The helminth holobiont: a multidimensional host–parasite–microbiota interaction
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Citation Excerpt :
Currently, infections with gastrointestinal (GI) helminths, including roundworms (e.g., Ascaris lumbricoides, Strongyloides stercoralis), hookworms (e.g., Ancylostoma spp., Necator americanus), whipworms (e.g., Trichuris trichiura), affect ∼2 billion people worldwide, resulting in a disease burden of tens of millions of disability-adjusted life years (DALYs) [1]. In farm animals, helminths (e.g., Haemonchus contortus, Teladorsagia circumcincta, Anoplocephala perfoliata) are responsible for devastating production traits and economic losses due to the extensive morbidity and mortality associated with infections and thus represent a major global veterinary health concern [2]. Control of infections in both humans and animals currently relies on the administration of anthelmintic drugs.
Gastrointestinal helminths have developed multiple mechanisms by which they manipulate the host microbiome to make a favorable environment for their long-term survival. While the impact of helminth infections on vertebrate host immunity and its gut microbiota is relatively well studied, little is known about the structure and functioning of microbial populations supported by metazoan parasites. Here we argue that an integrated understanding of the helminth-associated microbiome and its role in the host disease pathogenesis may facilitate the discovery of specific microbial and/or genetic patterns critical for parasite biology and subsequently pave the way for the development of alternative control strategies against parasites and parasitic disease.
To treat or not to treat: diagnostic thresholds in subclinical helminth infections of cattle
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Helminth infections of cattle place significant burdens on livestock production and farm economic efficiency. Heavy infections are relatively easy to detect and treat with anthelmintics. However, subclinical infections have major but often hidden impacts on animals, necessitating more refined diagnostics to detect them and ideally inform farmers about the likely impact of anthelmintic treatment on animal and herd performance. Here, we review recent advances in diagnosing three major cattle helminth infections – gastrointestinal nematodes (GINs), liver flukes, and lungworms – and the search for subclinical infection thresholds to guide treatment decisions. Combining refined diagnostic thresholds with farm-specific information on grazing systems and animal history enables farmers to tailor helminth treatments to specific epidemiological circumstances, thereby limiting anthelmintic resistance (AR) and boosting agricultural efficiency and food security.
Generalist nematodes dominate the nemabiome of roe deer in sympatry with sheep at a regional level
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The growth of livestock farming and the recent expansion of wild ungulate populations in Europe favor opportunities for direct and/or indirect cross-transmission of pathogens. Comparatively few studies have investigated the epidemiology of gastro-intestinal nematode parasites, an ubiquitous and important community of parasites of ungulates, at the wildlife/livestock interface. In this study, we aimed to assess the influence of livestock proximity on the gastrointestinal nematode community of roe deer in a rural landscape located in southern France. Using ITS-2 rDNA nemabiome metabarcoding on fecal larvae, we analysed the gastrointestinal nematode communities of roe deer and sheep. In addition, we investigated Haemonchus contortus nad4 mtDNA diversity to specifically test parasite circulation among domestic and wild host populations. The dominant gastrointestinal nematode species found in both the roe deer and sheep were generalist species commonly found in small ruminant livestock (e.g. H. contortus), whereas the more specialised wild cervid nematode species (e.g. Ostertagia leptospicularis) were only present at low frequencies. This is in marked contrast with previous studies that found the nemabiomes of wild cervid populations to be dominated by cervid specialist nematode species. In addition, the lack of genetic structure of the nad4 mtDNA of H. contortus populations between host species suggests circulation of gastrointestinal nematodes between roe deer and sheep. The risk of contact with livestock only has a small influence on the nemabiome of roe deer, suggesting the parasite population of roe deer has been displaced by generalist livestock parasites due to many decades of sheep farming, not only for deer grazing close to pastures, but also at a larger regional scale. We also observed some seasonal variation in the nemabiome composition of roe deer. Overall, our results demonstrate significant exchange of gastrointestinal nematodes between domestic and wild ungulates, with generalist species spilling over from domestic ungulates dominating wild cervid parasite communities.
Tracking gastrointestinal nematode risk on cattle farms through pasture contamination mapping
2022, International Journal for Parasitology
Citation Excerpt :
This has prompted the increased promotion of integrated parasite management (IPM) strategies. The ultimate aim of IPM strategies is the limitation of parasite burdens and delay of AR development through the careful implementation of chemotherapeutic or non-chemotherapeutic alternatives (Charlier et al., 2014; Morgan et al., 2019). Important to AR prevention is the development and maintenance of in refugia populations (van Wyk, 2001; Hodgkinson et al., 2019), whereby subpopulations of free-living stages on pasture or stages residing in hosts which have not received anthelmintic treatment are able to complete their lifecycle.
Gastrointestinal nematode (GIN) parasites in grazing cattle are a major cause of production loss and their control is increasingly difficult due to anthelmintic resistance and climate change. Rotational grazing can support control and decrease reliance on chemical intervention, but is often complex due to the need to track grazing periods and infection levels, and the effect of weather on larval availability. In this paper, a simulation model was developed to predict the availability of infective larvae of the bovine GIN, Ostertagia ostertagi, at the level of individual pastures. The model was applied within a complex rotational grazing system and successfully reproduced observed variation in larval density between fields and over time. Four groups of cattle in their second grazing season (n = 44) were followed throughout the temperate grazing season with regular assessment of GIN faecal egg counts, which were dominated by O. ostertagi, animal weight and recording of field rotations. Each group of cattle was rotationally grazed on six group-specific fields throughout the 2019 grazing season. Maps and calendars were produced to illustrate the change in pasture infectivity (density of L3 on herbage) across the 24 separate grazing fields. Simulations predicted differences in pasture contamination levels in relation to the timing of grazing and the return period. A proportion of L3 was predicted to persist on herbage over winter, declining to similar intensities across fields before the start of the following grazing season, irrespective of contamination levels in the previous year. Model predictions showed good agreement with pasture larval counts. The model also simulated differences in seasonal pasture infectivity under rotational grazing in systems that differed in temperature and rainfall profiles. Further application could support individual farm decisions on evasive grazing and refugia management, and improved regional evaluation of optimal grazing strategies for parasite control. The integration of weather and livestock movement is inherent to the model, and facilitates consideration of climate change adaptation through improved disease control.

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Trends in Parasitology

Feature Review100 Questions in Livestock Helminthology Research

Highlights

Section snippets

Towards Inclusive Identification of Research Priorities

Hypobiosis

Section II. Economic and Environmental Impacts

Section III. Effects on Host Behaviour and Welfare

Section IV. Host–Helminth–Microbiome Interactions

Section V. Host Resistance, Resilience, and Selective Breeding

Section VI. Development and Detection of Anthelmintic Resistance

When to Intervene against Resistance

Section VIII. Vaccines and Immunology

Plant-based Control

New Decision Support Tools for Helminth Control

Concluding Remarks

Acknowledgments

Glossary

Vet. Parasitol.

Trends Parasitol.

Vet. Parasitol.

Adv. Parasitol.

Biotechnol. Adv.

Vet. Parasitol.

Int. J. Parasitol. Parasites Wildl.

Trends Parasitol.

Livest. Sci.

Vet. Parasitol.

Adv. Anim. Biosci.

Environ. Toxicol. Pharmacol.

Sci. Total Environ.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Trends Parasitol.

Curr. Opin. Microbiol.

Trends Parasitol.

Vaccine

Vet. Parasitol.

Int. J. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Trends Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Int. J. Parasitol. Drugs Drug Resist.

Vet. Parasitol.

Vet. Parasitol.

Int. J. Parasitol. Drugs Drug Res.

Int. J. Parasitol.

Ecol. Model.

Vet. Parasitol.

Trends Parasitol.

Vet. Parasitol.

J. Pharm. Biomed. Anal.

Vet. Parasitol.

Vet. Immunol. Immunopathol.

Vet. Parasitol.

Small Rumin. Res.

Vet. Parasitol.

J. Invert. Pathol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Feature Review
100 Questions in Livestock Helminthology Research