1. Introduction

The equine bloodworm Strongylus vulgaris is regarded as the most pathogenic equine gastrointestinal helminth. The prevalence was reported to be 80%–100%, but decades of routine deworming has reduced its occurrence to very low levels. Most horses present with an acute peritonitis as the primary finding. Fecal egg counts have no diagnostic value in such cases, and a coproculture will only allow detection of adult parasites in the intestinal lumen, not the migrating larvae that cause the condition. The diagnosis of S. vulgaris-associated intestinal infarction is made by exploratory laparotomy, and the only curative treatment is resection of the infarcted tissue, where possible (Nielsen, 2019).

2. Aetiology

2.1 Parasitic characteristics

Adult S. vulgaris measure up to approximately 16 mm (males) and 24 mm (females) in length. They have a prominent buccal capsule with small teeth around its opening, a dorsal gutter, and two rounded teeth at its base. The copulatory bursa of the male is also prominent, and some elements of the alimentary and reproductive systems are usually obvious microscopically.

Eggs of S. vulgaris are typical "strongyle" eggs, oval, with a thin, smooth shell and measure approximately 90 µm by 50 µm. In fresh feces each egg contains a small clump of cells (a "morula"). Eggs of S. vulgaris cannot be differentiated microscopically from those of the other species of Strongylus, or from those of the non-migratory large strongyles, or of the cyathostomins (USask, 2021).

2.2 Classification

S. vulgaris, together with S. edentatus and S. equinus, are grouped as the migratory large strongyles of horses on the basis of the relative size of the adults and the extensive migrations of the developing larvae in the horse. The other groups of GI nematodes of horses are the large, non-migratory strongyles, and the small strongyles, also known as the trichonemes, cyathostomes, or more usually now, the cyathostomins (Roberts, 2005).

2.3 Life cycle 

Equine cyathostomes can undergo arrested development in the large intestinal mucosa for more than two years. Occasionally, these nematodes cause larval cyathostominosis, associated with weight loss and severe, persistent diarrhea and enteritis, which results from mass reactivation of inhibited cyathostomin larvae residing in the intestinal mucosa and the sudden release of large numbers of the larval stages of small strongyles. The clinical signs of cyathostominosis may be seen seasonally in autumn and spring, or may be brought about by the administration of anthelmintics to remove the luminal stages of small strongyles. Drug resistance of small strongyles to all classes of available antiparasitic compounds – except the macrocyclic lactones (ivermectin and moxidectin) – is a limiting factor in controlling these parasites and may result in an increased prevalence of clinical cyathostominosis over time. 

Despite enormous investments in the control of horse parasites, progress on the development of a diagnostic test has been very limited. Indeed, diagnosis of prepatent stages of cyathostomins in horses has always been difficult. Faecal worm egg count is available for determining the level of infection in individual horses. However, faecal testing can be negative, despite the presence of adult and larval stage four (L4) larvae in the faeces. A serological test based on immunoglobulin G (IgG) responses to larval antigen complexes has been reported. However, this test doesn’t allow prediction of a horse with cyathostomes (Elsheikha and Hallowell, 2014).

3. Epidemiology

3.1 Overall

Other than the longer pre-patent periods of Strongylus spp. and the non-migratory large strongyles, their basic epidemiology is in some ways similar to that of the cyathostomins.  Horses need access to pasture for significant parasite transmission to occur, and the longer pre-patent periods means that Strongylus spp. and the non-migratory large strongyles have essentially annual cycles (ingestion of infective larvae one year produces adults the next year), whereas adult cyathostomins could develop the same year and begin to contaminate the pastures with eggs towards the end of summer, depending on the local climate and its effects on the temperature-dependent egg development rates.  Under ideal conditions, the eggs of all these strongyles can develop to infective third-stage larvae in approximately one week. Where there is very little or no over-winter survival of the free-living stages of the parasites on pastures the major source of these parasites for grazing foals is the mares and other older and adult horses with which they are pastured. Where there is over-winter survival, the pastures could act as a source of infection (USask, 2021).

3.2 Environment factors

Strongyle egg output is known to vary seasonally. In Britain, Poynter found that minimal egg production occurred in winter, rising during the spring with maximal production in August or September (Poynter, 1954). In Ontario, Slocombe and McCraw also found that strongyle egg counts were high in August but during the period May to July counts were lower for thoroughbred, standardbred and show horses than for pleasure or commercial animals. Management and the time of administration of anthelmintics probably accounted for these differences. Following Poynter's study, Ogbourne showed that the percent of S. vulgaris (and S. edentatus) viable eggs was lowest in winter but reached a peak in May and remained high during the summer (Ogbourne, 1971). Thus, seasonal variations in adult populations of S. vulgaris (and S. edentatus) could be accounted for by seasonal differences in infection rate and the lengths of the prepatent periods (McCraw and Slocombe, 1976).

4. Pathogenesis

Within two days of infection Duncan and Pirie observed hemorrhagic foci on the mucosa of the ileum, cecum and colon. By one week post infection (PI) these authors noted a severe inflammatory reaction in the submucosa, with widespread arteritis, accompanied by thrombosis and infiltration by neutrophils. These changes were correlated with the molt of larvae to the fourth stage and soon extended to the muscularis and serosa. Infarction of the ileum, cecum and colon is observed two to three weeks PI along with thrombosis and thickening of the cranial mesenteric artery and its branches (Duncan and Pirie, 1975). At about this time tortuous fibrin tracts, often thread-like and so characteristic of early S. vulgaris infection, are observed on the intima of arteries and these may extend into the abdominal aorta (Figure 4). The tracks are overgrown with endothelium. Between one and four months PI the predominant lesions are in the cranial mesenteric and ileo-ceco-colic arteries, where the principal changes are thrombus formation and marked infiltration and fibrosis of the tunica media. Fourth stage, and later fifth stage larvae are associated with thrombi. Larvae returning to the intestine become encapsulated in nodules. Approximately nine months after infection with S. vulgaris larvae, a considerable reduction of lesions in the cranial mesenteric artery was found, suggesting that repair to earlier damage caused by larvae may occur (Duncan and Pirie, 1972).

Lesions brought about by S. vulgaris are most common in the cranial mesenteric and ileo-ceco-colic arteries (Ottaway and Bingham, 1946). A study found the incidence to be 86% in the cranial mesenteric artery followed by 62.5% in the cecal and colic arteries. Colic has long been considered related to thrombosis or embolism in these vessels. Aneurysms, especially of the cranial mesenteric artery, are often mentioned in the literature but a true aneurysm associated with S. vulgaris infection is rare if it occurs at all. While the lumen of an affected artery is often wider than normal the wall of the vessel is generally thicker (Figure 5) and the lumen of extensive sections of an artery may be several times its normal diameter. In older horses the cranial mesenteric and ileo-ceco-colic arteries are often encased in a large nodular mass. Within five or six weeks following infection, the intimal surface of the cecal and ventral colic arteries is often rough and may have a corrugated appearance (Figure 6).

Lesions in remote or unusual sites have been associated with S. vulgaris larvae. Cronin and Leader recorded a case of occlusion of the right coronary artery which they considered due to S. vulgaris larvae (Cronin and Leader, 1952). S. vulgaris in the A kidney is recorded. Intermittent lameness has been attributed to thrombosis or embolism of the external iliac artery, brought about by verminous arteritis. In a study of several cases of equids with neurological signs, S. vulgaris was suspected as an important cause of cerebrospinal nematodiasis. Little et al later induced signs and lesions of acute verminous encephalitis by inoculation of fourth and fifth stage S. vulgaris into the internal carotid artery of ponies (Little et al., 1974).

5. Clinical signs 

Typically, S. vulgaris-associated disease is a nonstrangulating intestinal infarction presenting as peritonitis and accompanied by these clinical signs:

• Fever
• Decreased or absent borborygmus
• Hyperemic mucous membranes
• Normal to slightly elevated heart rate
• No or mild pain
• Negative gastric reflux
• A sore mass palpable on rectal examination

Clinical laboratory findings typically include:

• Increased serum amyloid A and fibrinogen concentrations
• Decreased plasma iron concentration
• Leukopenia
• Increased lactate in plasma and peritoneal fluid
• Abdominocentesis reveals a fulminant peritonitis with high numbers of white blood cells and increased protein and lactate content.

Infection with S vulgaris will invariably cause a chronic-active verminous end-arteritis in the mesenteric arteries, but this has not been associated with a distinct clinical syndrome. Similarly, no clinical signs have been linked to the formation and subsequent rupture of the intestinal abscesses. Finally, although adult S. vulgaris parasites can be found attached to the intestinal walls and are described to ingest blood, they rarely, if ever, are the primary cause of clinical anemia.  

6. Diagnosis

6.1 Postmortem examination

The diagnosis of S. vulgaris-associated colic is invariably retrospective and is often possible only after surgery or postmortem examination. Horses with nonstrangulating infarction of the cecum or colon carry a guarded prognosis, as the presence of a cranial mesenteric thrombus may lead to further thromboembolic events. Spasmodic colic episodes that resolve with medical treatment in horses with a history of poor worm control may be attributable to S. vulgaris infection. Fecal worm egg counts will identify strongylid eggs, but differentiation between S. vulgaris and cyathostomin larvae is possible only by larval culture. Knowledge of poor parasite control (monitored by periodic fecal egg count) on the farm of origin may raise the index of suspicion for this disease. Treatment of proven S. vulgaris infection is straightforward as the parasite is sensitive to most modern anthelmintics (White et al., 2009).  

6.2 Exploratory laparotomy

A nonstrangulating intestinal infarction can only be diagnosed by exploratory laparotomy. Fecal flotation and egg counts have no diagnostic value. A coproculture allows identification of third-stage larvae and can help diagnose the presence of adult parasites in the intestinal lumen. However, this has limited value because the condition is not caused by adult parasites but by migrating larvae (Nielsen, 2019).

6.3 Abdominocentesis

Abdominocentesis is required to diagnose the peritonitis. In areas where S. vulgaris is endemic, a nonstrangulating intestinal infarction should be considered in cases presenting with peritonitis (Nielsen, 2019).

7. Treatment

            Once intestinal infarction is diagnosed, surgical correction should followimmediately. This should include:

• Resection of infarcted intestinal tissue
• Removal of adherences
• Medical treatment is generally not successful. Exploratory laparotomy reveals the extent of intestinal lesions and allows determination of whether surgical correction is feasible. The prognosis for patients found eligible for corrective surgery is good to excellent. In comparison, the prognosis is guarded if surgery is attempted >24 hours after onset of clinical signs.

Standard postsurgical care includes:

• Fluid therapy
• Anti-inflammatory therapy
• Antibiotics
• There is little or no value in administering anthelmintic medication in the acute phase of a nonstrangulating intestinal infarction. However, deworming with a larvicidal anthelmintic is recommended once the patient is stabilized and peritonitis has been resolved. This can be either ivermectin (0.2 mg/kg), moxidectin (0.4 mg/kg), or a 5-day course of fenbendazole (10 mg/kg) (Nielsen, 2019).

8. Control and prevention

Strategies to decelerate further selection for drug resistance, thereby extending the lifetime of currently effective anthelmintics should be implemented whenever possible. Recipe-based treatment programmes based solely on the calendar without regard to the medical needs of individual horses, the biology of the parasites or whether the drug is actually effective against the target parasites can no longer be justified or recommended. An evidence-based approach must be adopted in which the biology of the target parasites and effectiveness of drugs are considered and each horse is viewed as an individual patient with individual medical needs. 

To develop such a programme we must: 1) follow epidemiological principles of nematode control; 2) determine which drugs are effective on each farm; 3) use the correct drug for the correct parasite developmental stage at the appropriate time of the year; 4) determine which horses require less or more frequent treatment by performing FEC ‒ faecal egg counts); and 5) evaluate the overall success of the worm control programme by monitoring the FEC of all horses on the property at regular intervals. 

In the course of recent studies investigating the prevalence of anthelmintic resistance we have met many horse owners who refuse to adjust their normal deworming routine even when shown results of FEC that are negative. This attitude commonly held by horse owners stems partly from the belief that all worms are bad and that no worms should be tolerated in a horse. This attitude is also influenced by the widely held notion that all horses are highly susceptible to worms and, therefore, all horses should be treated the same. However, these notions are both completely false. Horses evolved with their intestinal worms and small numbers of most worms do not cause any significant health impairment, but rather help to stimulate immunity that serves to protect the horse from the establishment of a more serious worm burden. Furthermore, small numbers of eggs shed by untreated horses are critical for slowing the development of anthelmintic resistance (details below). Finally, all horses are not the same. Parasite burdens are highly aggregated in hosts, meaning that about 20–30% of horses harbor about 80% of all the worms. On many farms this distribution is skewed even further. Thus, some horses consistently shed extremely high egg numbers even when treated frequently with anthelmintics while other horses have strong immunity and consistently shed very low numbers of eggs (Kaplan and Nielsen, 2010).

9. References

AbouLaila, M., Allam, T., Roshdey, T., Elkhatam, A.J.V.P.R.S., Reports, 2020. Strongylus vulgaris: Infection rate and molecular characterization from naturally infected donkeys at Sadat City, Egypt.  22, 100478.

Cronin, M., Leader, G.J.V.R., 1952. Coronary occlusion in a thoroughbred colt. 64.

Duncan, J., Pirie, H.J.R.i.v.s., 1972. The life cycle of Strongylus vulgaris in the horse.  13, 374-385.

Duncan, J., Pirie, H.J.R.i.V.S., 1975. The pathogenesis of single experimental infections with Strongylus vulgaris in foals.  18, 82-93.

Elsheikha, H.M., Hallowell, G.J.V.T., 2014. Strongylosis in equines: biology, diagnosis and future needs.  44, 27-30.

Kaplan, R., Nielsen, M.J.E.V.E., 2010. An evidence‐based approach to equine parasite control: It ain't the 60s anymore.  22, 306-316.

Little, P., Lwin, U., Fretz, P.J.A.j.o.v.r., 1974. Verminous encephalitis of horses: experimental induction with Strongylus vulgaris larvae.  35, 1501-1510.

McCraw, B.M., Slocombe, J.O., 1976. Strongylus vulgaris in the horse: a review. The Canadian veterinary journal = La revue veterinaire canadienne 17, 150-157.

Nielsen, M.K., 2019. Strongylus vulgaris-Associated Disease in Horses. MSD Manual. Veterinary Manual.

Ogbourne, C.J.P., 1971. Variations in the fecundity of strongylid worms of the horse. 63, 289-298.

Ottaway, C., Bingham, M.J.V.R., 1946. Further observations on the incidence of parasitic aneurysm in the horse.  58, 155-159.

Poynter, D.J.V.R., 1954. Seasonal fluctuation in the number of strongyle eggs passed by horses.  66, 74-78.

Roberts, L.S.J.J., seventh edition McGraw Hill, 2005. John Janovy Foundations of Parasitology. 279-283.

USask, 2021. Strongylus vulgaris. Western College of Veterinary Medicine 

White, N.A., Moore, J.N., Mair, T.S., 2009. Equine acute abdomen. CRC Press.