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Biology and Life Cycles of Equine Parasites

Life cycles are the road maps that guide parasites to their ultimate goal - propagating a subsequent generation. Some parasites follow a single, direct path to grandma's house, while yet others may travel by convoluted routes, sojourn for protracted periods at some wayside convenience, or even pick up a passenger or two. These differences represent alternate strategies for coping with the vagaries of the environment and of their eventual hosts.

A thorough knowledge of life cycles is not emphasized merely to torment veterinary students. Rather, life cycle details reveal opportunities to control parasites through chemical or management interventions, to exploit unfavorable environmental conditions, or to promote natural enemies that might act as agents of biological control. Taking advantage of these potential control opportunities will be emphasized in individual chapters in this volume.

At the root of all life cycles is a fundamental principle that distinguishes helminth parasites from other infectious agents such as viruses, bacteria, fungi, and protozoa. Through various types of clonal expansion, the latter can all amplify their numbers within a host animal. Literally millions of individual organisms may arise from infective burdens that are orders of magnitude smaller. The reproductive products of nearly all helminths, however, are required to leave the host and undergo essential change in a different location. Defecation is the most common means by which reproductive products exit the host, but a notable exception includes immature parasitic stages that are ingested by blood-sucking arthropods (e.g., Onchocerca, Setaria). Most parasitic products can become infective in the environment, whereas others require intermediate hosts or vectors. Regardless, all of these essential transformations occur "outside the definitive host". Indeed, dramatic biological change is mandatory before a parasitic organism is capable of infecting a new host animal or of reinfecting the original host.

Compared to those organisms that amplify their numbers through clonal expansion, helminth disease is a numbers game. Simply put, as the number of invading parasites increases, greater tissue damage or nutrient loss results, and the range and severity of clinical signs become more extensive.

In this chapter, we propose to describe the basic life cycles of the major helminth parasites of equids. Specific control opportunities may be mentioned in this overview, but these will be discussed more fully elsewhere in the volume.

Nematodes

Superfamily Strongyloidea

The members of the Strongyloidea ("strongyles") are moderately sized, stout worms with substantial buccal capsules. The males have a copulatory bursa at the posterior end and females of all species produce eggs that are similar in appearance. Eggs of small strongyles cannot be differentiated microscopically from those of large strongyles, and the only practical method of differentiation (other than molecular approaches) is through coproculture. The strongyloids of horses all have direct life cycles; intermediate or paratenic hosts are never used (Figure 1.1).

Figure 1.1 Strongyle life cycle. The life cycle of strongyle parasites. Parasitic stages can be seen above the horse and preparasitic stages below it. Fertilized eggs are shed by adult females in the cecum and colon, and excreted to the environment in the feces. Here, the eggs hatch and a first-stage larva (L1) emerges. The L1 then molts to L2 in the feces. Another molt gives rise to the L3, which retains its L2 cuticle and thus has a double-layered sheath. The L3 leaves the fecal pat and migrates on to forage, where it is ingested by a horse. Inside the horse, the L3 exsheathes and invades the mucosa of the large intestine. Large strongyles (Strongylus spp.) undergo extensive migration in various organs of the horse, while cyathostomins encyst in the mucosal lining of the large intestine. After returning to the large intestinal lumen, the worms reach sexual maturity and start shedding eggs.

Strongyloid eggs pass in feces and hatch in favorable environmental conditions of moisture, temperature, and oxygenation. All species exhibit three sequential larval stages, first (L1), second (L2), and third (L3). The L1 and L2 stages feed on organic material in the environment, but the third stage develops within the sheath of the L2. This protective covering helps L3s to resistant environmental conditions, but it has no oral opening, so third stage larvae are unable to ingest nutrients. The L3 is the infective stage for all strongyloid nematodes of equids. Infection invariably occurs through inadvertent ingestion, whether while grazing or via oral contact with elements of the environment.

Apparently, horses never develop absolute immunity to strongyloids, so these are often the sole nematode parasites recovered from well-managed, mature equids. The Strongyloidea of horses are comprised of two distinct subfamilies, the Strongylinae and the Cyathostominae.

Strongylinae (large strongyles)

Members of the subclass Strongylinae tend to be larger, on average, than most genera that comprise the Cyathostominae. In addition, Strongylinae have large buccal capsules, adapted for attachment to, and even ingestion of, the gut mucosa. The larval stages of at least one strongylin genus undergo extensive, albeit stereotypic, migration within the host prior to returning to the gut to mature and begin reproduction.

Strongylus vulgaris

Strongylus vulgaris is widely acknowledged as the single most pathogenic nematode parasite of horses. Adult worms measure about 1.5-2.5?cm in length and the females are larger than the males. Adults are usually found attached to the mucosa of the cecum and the ventral colon (Figure 1.2). After ingestion from the environment, third stage larvae invade the mucosa of the distal small intestine, cecum, and colon. Here, they molt to the fourth stage (L4) before penetrating local arterioles and migrating proximally beneath the intimal layer of local blood vessels. Migrating S. vulgaris L4s leave subintimal tracts in their wake and congregate near the root of the cranial mesenteric artery. A portion of the infecting larvae may continue to migrate, even to the root of the aorta near the left ventricle. Migrating L4s have been found in numerous vessels arising from the aorta, including the celiac artery, the renal arteries, and external and internal iliac arteries. The pathologic characteristics and consequences of these arterial lesions will be discussed in Chapter 2.

Figure 1.2 Adult Strongylus vulgaris attached to the cecal mucosa.

(Source: Photograph courtesy of Dr. Tetiana Kuzmina).

Larvae reach the cranial mesenteric artery about two weeks post-infection. Here, they reside for about four months before returning to the large intestine. The final molt to the L5 stage occurs about 90 days after infection, while larvae are still present in the artery. These L5s (essentially young adults) characteristically retain their L4 cuticle and thus appear with a double-layered cuticle just like the infective L3 (Figure 1.3). Beginning approximately 120 days after infection, young adults migrate within the blood stream to the large intestine, where they are found within pea-sized nodules in the submucosa of the ventral colon and cecum. Adult worms eventually emerge from these nodules and mature in the intestinal lumen for an additional 6 weeks. Females begin to lay eggs from 5.5 to 7 months after infection (Ogbourne and Duncan, 1985).

Figure 1.3 Strongylus vulgaris L5 pre-adult collected from the cranial mesenteric artery. Note that this specimen characteristically has retained its L4 cuticle.

Strongylus edentatus

Strongylus edentatus is a larger worm than S. vulgaris, measuring about 2.5-4.5?cm in length, and apparently is also more prevalent. Adults are usually attached to the mucosa of the base of the cecum and the proximal ventral colon. The larvae undergo a complex and fascinating migratory route. Following ingestion of infective L3 stages from the environment, larvae are carried by the portal system to the liver, where they molt to the fourth stage. Following migration within the parenchyma, larvae leave the liver via the hepatorenal ligament and migrate beneath the peritoneum to various locations in the flanks and ventral abdominal wall (hence, the common term, "flank worm"). Larvae are also commonly found in the perirenal fat. The majority of larvae are found on the right side of the body (i.e., in the right ventral abdominal wall and around the right kidney), probably because the hepatorenal ligament attaches on the right side of the ventral midline (see Chapter 2).

The final molt to the fifth stage occurs within retroperitoneal nodules about four months post-infection. Young adults migrate back to the large intestinal walls (primarily the ventral colon), where purulent nodules form and eventually rupture to release adult worms into the lumen. Altogether, this extensive migration results in a prepatent period of up to one year (McCraw and Slocombe, 1978).

Strongylus...