While equids can be affected by both endo- and ecto-parasites, the greatest welfare and productivity burden comes from endoparasitism. Most horses exposed to pasture will be infected with gastrointestinal helminths, normally at a level that allows benign coexistence without development of clinical disease. However, there is always the potential for high worm burdens to accumulate and manifest clinically as life-threatening disease, especially in immunocompromised or naïve individuals kept on densely-stocked and poorly managed pastures.
Common clinical signs associated with gastrointestinal parasitism include failure to thrive, abdominal distension and pain, diarrhoea and weight loss, with more specific manifestations linked to particular parasitic infections (Saeed et al, 2019). This potential pathogenicity has driven widespread adoption of preventative control measures, historically through population-wide administration of anthelmintic drugs at regular dosing intervals. Although extensive availability of anthelmintic drugs has changed the landscape of pathogenic parasite species, it has come at the cost of increasing development of anthelmintic resistance, which threatens to undermine control options and once again alter the parasites posing the greatest threat to equine populations (Nielsen, 2022). Through an understanding of the evolution of parasite control, it is possible to appreciate parasite species of importance, past and present, and recognise currently minor species that could rise to significance in the future.
Evolution of parasite control
During the 1960s, the introduction of benzimidazole anthelmintic drugs to the market allowed the first clear recommendations with regard to control of endoparasites in equids to be made (Silva et al, 2019; Rendle et al, 2024). These recommendations were largely aimed at controlling the large strongyle, Strongylus vulgaris (S. vulgaris), at the time regarded to be the most pathogenic parasite of equids. Equine anthelmintics have evolved from early benzimidazoles and organophosphates to include the currently licensed classes: benzimidazoles (eg Fenbendazole), tetrahydropyrimidines (eg Pyrantel) and macrocyclic lactones (eg Ivermectin and Moxidectin) (Merlin et al, 2024a). Initial control strategies aimed to disrupt parasite lifecycles through indiscriminate anthelmintic use on all members of the population at 6–8-week calendar intervals (Silva et al, 2019). This was undeniably successful in significantly reducing incidence of clinical disease caused by S. vulgaris but has come at the cost of widespread development of anthelmintic resistance. Today, resistance to benzimadazoles and pyrimidine products is extensively reported in cyathostomins, with resistance to macrocyclic lactones also thought to be emerging as indicated by reducing egg reappearance periods for Ivermectin and Moxidectin. Egg reappearance periods were around 8–10 weeks for Ivermectin and 12–16 weeks for Moxidectin in the 1990s, both reduced to 5 weeks in studies published after 2000 (Nielsen, 2022). Conversely, ascarid species show widespread resistance to macrocyclic lactones, with more recent reports of emerging benzimadazole and pyrimidine resistance.
With no new anthelmintic products likely to reach the equine market, it is clear that interval control methods are unsustainable and need to be replaced by risk-based, diagnostic-led methods of anthelmintic treatment (Rendle et al, 2024), which just treat horses most at risk of clinical disease and with the highest worm burdens. This targeted treatment approach is based on the principles of overdispersion and refugia. As parasite infections show a negative binomial distribution in horse populations (Matthews et al, 2023), meaning that 20% of animals harbour 80% of parasites, treatment of just high shedders should significantly reduce anthelmintic use. In turn, a proportion of the population are left untreated and act as a source of refugia; subjecting unexposed parasites with genes that confer anthelmintic susceptibility to dilute resistant alleles and reducing selection pressure for drug resistance (Nielsen et al, 2014).
Targeted treatment relies on the accuracy of faecal worm egg counts to detect high-shedding animals, and there is no proven evidence that this ensures individual health and welfare. Some horses with low faecal worm egg counts may benefit from anthelmintic treatment as they may still harbour clinically significant parasite burdens, particularly in cases of encysted cyathostomins, which do not always shed detectable eggs (Uhlinger, 2007). This means that relying solely on faecal egg counts could miss these infections, potentially leading to health risks. The uncertainty in individual treatment outcomes has acted as a barrier to widespread adoption of targeted treatment strategies. It is now clear that other methods to reduce environmental contamination with infective larvae are needed. It is likely that a combination of strategies is the only route to long-term, effective and sustainable parasite control (Szewc et al, 2021).
Pasture management with regular removal of manure, quarantining and treatment of new arrivals before pasture turnout, co-grazing with other species and treatment with nematophagus fungi, are just some measures that could be used to reduce pasture prevalence of infective larvae. However, none of these measures are the panacea to effective control and potentially introduce new risks such as exposure to novel parasites from co-grazing species.
Cyathostomins
Cyathostomins, or small strongyles, are ubiquitous parasites, with almost all horses exposed to pasture being infected with one or more of the 50 identified species. They have a direct lifecycle with no intermediate host (Figure 1) and, although generally considered of low pathogenicity, with many horses harbouring large burdens without visible clinical effect, larval cyathostominosis is a severe potential sequalae with a 40–70% mortality rate (Corning, 2009). With interval anthelmintic treatment largely controlling disease caused by S. vulgaris, cyathostomins are currently considered the primary parasite affecting horses because of their high prevalence and increasing potential to cause disease in light of rising anthelmintic resistance (Matthews et al, 2023).
L3 larvae are the infective stage, ingested by the horse while grazing, but cyathostomin larvae have the ability to encyst within the mucosa of the caecum and large colon where they undergo hypobiosis, and can remain in a state of arrested development for up to 3 years (Walshe et al, 2020). Their ability to encyst within the intestinal walls allows large numbers of larvae to accumulate; while encysted, a fibrous capsule protects them from the host immune response and allows a state of balanced co-existence (Reinemeyer and Nielsen, 2009). However, to complete the lifecycle, excystment and removal of the fibrous capsule must occur. This leads to intense local inflammation and focal damage to the caecum and ventral colon, especially when larvae emerge synchronously in large numbers (Reinemeyer and Nielsen, 2009; Khan et al, 2015). It is this mass emergence of encysted larvae, often precipitated by anthelmintic administration (Rendle et al, 2024), that can lead to larval cyathostominosis.
Larval cyathostominosis is a protein-losing enteropathy (Bull et al, 2023) and colitis syndrome (Matthews et al, 2023) caused by the physical damage of, and immune and inflammatory reaction to, mass emergence of large numbers of encysted larvae. Clinically, it is characterised by diarrhoea, oedema, rapid weight loss, abdominal pain and hypoalbuminaemia. It has a seasonal occurrence, usually November–March in temperate climates, and although younger (<6 years) and older (>18 years) horses seem to be at higher risk (Rendle et al, 2024), horses of all ages can be affected (Corning, 2009). The increasing levels of anthelmintic resistance and limited availability of larvicidal drugs, presence of encysted larvae in arrested development and ability of L3 to overwinter in the environment (Matthews et al, 2023) mean control of these parasites is not simple, and eradication probably impossible.
Strongylus vulgaris
S. vulgaris was the archetypal pathogenic gastrointestinal parasite of horses, once considered a major cause of colic (Rendle et al, 2024). As a large strongyle, it has a similar life cycle to the small strongyles (Figure 1), but with the added characteristic of larval migration. The L3 infective stage is inadvertently ingested by horses during grazing (Khan et al, 2015); they then ex-sheath and invade the small intestinal submucosa where they moult to L4 (Reinemeyer and Nielsen, 2009). The L4 and L5 larval stages are responsible for the extra-intestinal migration which is characteristic of this parasite; entering local arterioles, invading beneath the vessel intima, before moving proximally to their typical location in the cranial mesenteric artery (Reinemeyer and Nielsen, 2009). L3 and L4 larval forms damage the intestinal mucosa and submucosa (Uhlinger, 2007), but the major pathological effect comes from 4 months of larval migration in the mesenteric arteries (Hedberg-Alm et al, 2020). As they migrate, larvae induce an endarteritis, with thickening of the arterial wall and thrombus formation; the detachment of which leads to obstruction of smaller downstream arterioles, ultimately leading to ischaemia of the intestinal segment supplied by these vessels (Tydén et al, 2019). This leads to the verminous arteritis, severe non-strangulating intestinal infarction and thromboembolic colic, which is often fatal and regarded synonymous with S. vulgaris infection.
As a result of extensive adoption of regular interval dosing with broad-spectrum anthelmintics, reductions in prevalence of S. vulgaris infections have been reported worldwide (Pilo et al, 2012), with thromboembolic colic becoming a near forgotten condition. However, a post-mortem study in Sardinia showed presence of S. vulgaris lesions in the cranial mesenteric artery of all 46 horses examined; indicating the parasite is still very much present in horse populations (Pilo et al, 2012). Additionally, anthelmintic drugs have been made prescription-only in Sweden since 2007 as a result of rising levels of anthelmintic resistance (Tydén et al, 2019). This has led to evidence of remaining infection pressure by S. vulgaris. Osterman-Lind et al (2023) reported that 53% of equestrian premises studied had at least one horse infected with S. vulgaris in 2015, compared to just 6% in 2008. Tydén et al (2019) observed a 2.9x increased odds of infection on farms using faecal egg count-directed anthelmintic treatment. This serves as precautionary evidence that S. vulgaris could resume its role as a significant parasite of horses with the move to more targeted anthelmintic dosing regimens.
Parascaris equorum
The ascarid parasite, Parascaris equorum (P. equorum), is the largest nematode to affect horses and found in the small intestine of youngsters (Reinemeyer and Nielsen, 2009). As a result of the development of an age-dependant, acquired immunity by about 6 months of age (Merlin et al, 2024b), patent infections are uncommonly found in adults (Abbas et al, 2023). Egg shedding shows a biphasic age-restricted pattern; peaking at 4 months, and again at 8–10 months old (Hautala et al, 2019; Rendle et al, 2024). Of note is the durability of P. equorum eggs; they are able to survive on pasture for 5–10 years (Reinemeyer, 2012) and represent an important source of infection for foal crops year on year, on intensively managed breeding premises.
P. equorum has a direct life cycle (Figure 2), the infective stage being a larvated egg, containing L2. Following ingestion during grazing, larvated eggs hatch in the small intestine and first enter the liver via the portal circulation where they undergo intra-hepatic migration, before entering the lungs and migrating up the respiratory tree to be swallowed (Reinemeyer and Nielsen, 2009; Saeed et al, 2019). Once back in the small intestine, they mature to adult worms in the duodenum and jejunum (Saeed et al, 2019). This hepatotracheal migration accounts for the ability of this parasite to cause respiratory signs such as nasal discharge and coughing, in addition to the more classical signs seen in most equine gastrointestinal helminth infections (Saeed et al, 2019). Although infection of youngsters with P. equorum is near ubiquitous, development of clinical disease is currently uncommon (Rendle et al, 2024). It is thought large worms, when viable, cause little effect on the intestines; however, if killed by an effective anthelmintic, they can lead to mechanical obstruction (Reinemeyer and Nielsen, 2009) and associated small intestinal impaction colic, sometimes progressing to fatal rupture. Future concern is for potential pathogenicity of this parasite in the face of anthelmintic resistance. The current extensive use of macrocyclic lactones on breeding farms has largely controlled clinical disease associated with ascarid impactions. However, with resistance to multiple classes of anthelmintics being reported in ascarids from several countries (Reinemeyer, 2012; Matthews, 2014; Abbas et al, 2024) clinical disease is likely to become increasingly prevalent.
Anoplocephala perfoliata
Tapeworm parasites that infect horses include Anoplocephala magna, Anoplocephala mamillana and Anoplocephala perfoliata (A. perfoliata). A. perfoliata is most commonly associated with clinical disease. According to equine post-mortem studies, tapeworm infection in the UK and Ireland has a reported prevalence of 51–69% (Rendle et al, 2024), although subtle effects on growth and productivity (Reinemeyer and Nielsen, 2009) are the most likely impact, rather than visible disease. Unlike many helminths, where it is the large size of the burden that can lead to clinical disease, infection with >20 A. perfoliata tapeworms puts the horse at risk of clinical sequalae (Matthews et al, 2023; Rendle et al, 2024).
A. perfoliata has an indirect lifecycle, involving oribatid mites as the intermediate host (Figure 3). Horses ingest oribatid mites containing the infective cysticercoid while grazing, which develop to adult tapeworms in the intestine. It is this parasite attachment to the intestinal mucosa that leads to pathology in the form of mucosal ulcerations, local inflammation and development of fibrous connective tissue (Reinemeyer and Nielsen, 2009). A. perfoliata has a predilection for attachment at the ileocaecal junction and has been associated with development of intussusceptions (Nielsen, 2016), as well as spasmodic colic (Hedberg-Alm et al, 2020). The exact pathogenesis of how A. perfoliata contributes to colic development is unknown, but suggestions include local inflammation adversely affecting gut motility, fibrous connective tissue at sites of parasite attachment physically obstructing the ileocaecal valve and neural alterations to regional ganglia (Reinemeyer and Nielsen, 2009).
Perhaps the key concern with regard to tapeworm infections in the changing world of anthelmintic resistance and targeted control measures is sporadic release of low numbers of eggs, making faecal worm egg counts an insensitive method for detection of tapeworm infections (Burcáková et al, 2023). This means that serum/saliva enzyme-linked immunosorbent assay tests must be added to any targeted control programme to ensure tapeworm infections are identified and treated before clinical disease results.
Strongyloides westeri
Strongyloides westeri is a nematode found in the small intestine of foals up to 16 weeks of age, most being infected with L3 from their dams via the transmammary route (Abbas et al, 2021). It is usually an inconsequential, self-limiting infection (Rendle et al, 2024), but can occasionally lead to acute enteritis, diarrhoea and dermatitis (Abbas et al, 2021). Experimental infection is not associated with clinical disease (Miller et al, 2017). Because of its rare pathogenicity, the routine practice of deworming foals during the first month of life has been suggested as obsolete (Reinemeyer, 2012) in light of growing anthelmintic resistance. However, Abbas et al (2021) caution over the potential for S. westeri prevalence to increase with future decreased use of macrocyclic lactones; in Kentucky, prevalence in foals was <6% in the late 1990s, but rose to 30% in 2014.
Oxyuris equi
Oxyuris equi, the equine pinworm, is an omnipresent parasite with a worldwide distribution. It has a unique direct lifecycle (Figure 4) with adults residing in the colon, before gravid females migrate to the anus where they deposit eggs in a white adhesive substance (Saeed et al, 2019). Although larval stages in the colon can cause mucosal ulcerations and inflammation, it is desiccation of the egg secretion substance at the anus that causes the classical clinical signs of tail rubbing and pruritis (Wolf et al, 2014; Saeed et al, 2019). Although generally regarded as a nuisance rather than a pathological concern, anecdotal reports suggest UK prevalence is increasing (Rendle et al, 2024). In Germany, Wolf et al (2014) reported two separate cases of persistent O. equi infection and continued egg shedding despite treatment with Ivermectin and Moxidectin. Although this is not definitive evidence of anthelmintic resistance, because of incomplete oxyuricidal efficacy of most anthelmintics (Reinemeyer, 2012), it is a reminder that parasite species regarded as of greatest importance in equids may change in the future.
Other parasites to consider
A plethora of parasites infect equids, the breadth of which cannot be explored in a single article. However, in addition to the main species already explored, a few others merit consideration in the climate of changing parasite control and increasing anthelmintic resistance development.
Fasciola hepatica is a liver fluke mainly affecting ruminants that can infect any species grazing wet pasture contaminated with snail intermediate hosts. A case-control study by Howell et al (2020) suggested that liver flukes may be an unrecognised cause of liver disease in horses and that co-grazing, as an alternative, more sustainable method of parasite control, could put horses at increased risk of fluke infection. Accordingly, F. hepatica could be a parasite to consider in the future, although their inability to develop a patent infection in horses (Howell et al, 2020) means that faecal worm egg counts are unlikely to be diagnostically helpful. Serological tests can be useful for diagnosis (Howell et al, 2020).
Onchocera cervicalis is a filarial nematode, more commonly referred to as the neck threadworm. It has an indirect lifecycle with culicoides midges acting as intermediate hosts, and adults residing in the nuchal ligament of horses for up to 15 years (Mansell and Behnke, 2022). Microfilariae produced by adults migrate through dermal connective tissues and cause severe pruritis and dermatitis (Mansell and Behnke, 2022). Although the threadworm has a worldwide distribution, it is currently considered insignificant in the UK as routine administration of Ivermectin and Moxidectin to control gastrointestinal nematodes inadvertently kills dermal microfilariae (Mansell and Behnke, 2022). However, as adults are not killed by macrocyclic lactones, it is only through regular anthelmintic administration that microfilariae and associated clinical signs are controlled. Additionally, with climate change increasing UK culicoides abundance (Mansell and Behnke, 2022), this is another species that could rise to future importance.
Ectoparasites
Horses can be affected by a wide variety of ectoparasites including mites, ticks and lice. Few have significant clinical impact beyond irritation, but perhaps more important in the state of increasing global temperatures and extensive global horse movement, are their ability to act as vectors for a multitude of other pathogens. For example, equine piroplasmosis caused by the protozoan parasites Babesia caballi and Theileria equi is endemic in most countries, but historically not in the UK because of a lack of suitable tick vectors. However, with vectors now reported and no legislation around import testing, the UK is at significant risk of disease incursion and establishment (Coultous et al, 2019).
Conclusions
Although there are key parasite species affecting horses, their relative importance and prevalence have changed and are likely to continue to change over time. The increasing development of anthelmintic resistance in combination with a lack of appropriate pasture management means that endoparasite-related problems are becoming an increasingly critical problem worldwide. Greater efforts are needed to encourage targeted anthelmintic use, improve non-chemical control measures and pasture management, and widen research into novel ways to control parasite infections.