3.1 Evolution of intestinal parasitic nematodes

The body of nematodes is elongated, circular in cross-section and without a circulatory system. The hydrostatic skeleton makes valves necessary for all body openings. Growth takes place by moulting without a decrease of the haemolymph pressure while the stretched cuticle is being shed. These circumstances determine the differentiation of all forms, for both free-living and parasitic types.

Intestinal parasitism by nematodes evolved polyphyletically. The many nematodes dwelling in the gastro-intestinal tract may be regarded as a typocological sequence involving the evolution from saprophytes free-living in the ground (e.g. Rhabditida) via commensales and finally to weakly parasitic types. The saprophytic forms live on bacteria in degrading composting plant material or in the excrement of herbivores representing a biochorion with rapidly changing external conditions. Commensal or weakly parasitic forms (e.g. Syphacia spec.), which live in large caeca containing food symbionts, are exposed to similar but nevertheless constant conditions, namely the decomposing masses of a substrate that, despite its low nutritional value, is permanently replaced and is easy to reach by the direct oral-enteral route.

Enterobius vermicularis, the human pinworm, lives in the rectum feeding on bacteria. The females carry out perianal oviposition by migrating around the anus, following an interfaecal diurnal cycle. This species represents an intestinal nematode without direct host tissue contact (see below).

The strongyloidea and trichostrongyloidea are differentiated to the specialized food and the digestive tract of ruminants. They adapt their population density by retarding their development (moults) in response to crowding and to the secretory immune reaction of the intestine. Eggs are excreted together with host faeces. Permanent stages bridge seasonal climate changes.

Strongyloides stercoralis propagates under favourable external conditions of a biochorion by free-living bisexual generation (heterogony); during food shortages, it becomes facultatively parasitic. In the mucosa of the duodenum of man, cat or dog, the females propagate parthenogenetically (homogony). They give rise to larvae that are capable of autoinfectivity. Depending on the body region in which the re-invasion occurs, the larvae take a percutanous or a transentero-somatic route.

Three species of Anisakidae of the piping hare (Ochotoma princeps) are adapted by diurnal migrations to the twofold passage of food, which consists of fresh green and caecotrophe, in leporidae (fig. 3.1, page 178).

Trichiuris trichiura, the whipworm of man: During prepatency, the invading first-stage larvae exert host tissue contact by temporary penetration into the villi of the gut epithelium. The adults live in the caecum. Their anterior part of the body penetrates several the cells of the gut epithelium, whereas the posterior part of the body extends into the lumen. By means of an oral stiletto, histolytic secretions are infused into the gut epithelium cells, the plasma of which is taken up orally.

Nippostrongylus brasiliensis, the hookworm of the rat: During prepatency, the invading larvae migrate through the mucosa into the muscularis remaining there for 8-9 days and exerting the first host tissue contact. Returning into the intestinal lumen, the third-stage larvae secrete antigens that ambivalently stimulate the immune reaction: Superinfestations are damped down (premunition). However, defence reactions against established stages are suppressed

In omnivores and even more in carnivores, the bacterial intestinal flora is comparably scarce and symbiontic protozoa are totally absent. Thus, the living conditions for commensal nematodes are demanding. The immigrating nematode stages are immediately confronted with the immune apparatus (Peyer’s plaques), which is particularly reactive in the intestines. They not only have to resist to its defensive reactions, but also have to intervene specifically with respect to their own requirements.

In intestinal nematodes of omnivores, the infestive stages follow a transentero-somatic invasion route as a rule: intestine-liver-lungs-intestine-passage (Ascaris spec.,fig. 3.2, page 179). In that of carnivores, a percutaneous-somatic invasion route has been developed (Ancylostomatidae, tab. 3.1, page 180): during prepatency, there is intensified host tissue contact that modifies the defensive components of the immune reaction towards a balancing coexistence. Thereby, humoral immune reactions may be used by the parasite as signals for self-regulation of its population density.

Additionally, a somatic invasion route enables the parasite to divert the migrating infesting larvae directly to the placenta and milk glands, in the case of a pregnant host. By skipping the originally attacked host, the parasite exerts a generative transmission. Overcrowding of the mother animal is thus

prevented and the parasite is distributed to several individuals of the next host generation: compensation of the age drift (see below). If percutaneous invasion takes place, a translympho-somatic route is used with similar options (fig. 3.3, page 181).

In directly transmitted lungworms of herbivores (Metastrongyloidea), the transentero-somatic invasion route ends in the lungs. The adult worms live in the bronchiae and the trachea. Their eggs continue along the route to the intestine to be excreted. A vaccine had been developed against Dictyocaulus viviparus, the lungworm of cattle. However, the protective effect vanishes without continous stimulation (premunition).

After the penetration of the epithelium of the skin or intestinal tract, first contact with the immune system takes place in the regional lymph nodes (fig. 3.4 and 3.5, pages 182 and 183). After a latency of a few days, a delayed type hypersensitivity (DTH) is provoked in all cases but persisting protective immunity is never achieved. A premunition simulates a defence reaction but is only effective as long as living parasites are present, an analogy to the territorial defence behaviour of free-living animals.

Generative transmission (table 3.1, page 180) compensates the age drift that a parasite inevitably experiences (either directly or statistically) if it lives for a long time in relation to the life expectancy of its host, i.e. passing several propagation cycles of the latter. This is relevant when the parasite has a chance to attack the same host individual several times as a result of a balanced and therefore non-protecting immunity. Consequently, the hypothesis of an arms race between host and parasite should be replaced by that of a balance of power. This is characterized by the self-control of the propagation of the parasite based on inter- and intraspecific feed-back mechanisms.Ancylostoma duodenalis (fig. 3.6, page 185), A. caninum, Necator americanus, the hookworms of man and dog, respectively, feed on blood and intestinal tissue. They infest their hosts by percutaneous-somatic invasion. In pregnant dogs, the invading third-stage larvae of A. caninum are transmitted generatively via the placenta and, after litter production, by lactation. - In the fur seal (Callorhinus ursinus), hookworms (Uncinaria lucasi) reach the newborn by galactogenic transmission and then later attacks the same litter a second time by percutaneous invasion (fig. 8.2, page 283). Thereby, the hookworm synchronizes its propagation to that of the host. The oral-faecal transmission route of the earlier terrestrial evolutionary forms is completely avoided; this represents an adaptation to the marine environment of the host. Cyclic transmission: in order to change host, the nematode stages (eggs, larvae) sometimes use transporting hosts, which may develop into intermediate hosts thus leading to sophisticated nematode life cycles. - Angiostrongylus cantonensis, which lives in the lung arteries of the rat, uses 20 different terrestrial snails as intermediate hosts. The first-stage larvae evacuated in the rats’ faeces survive on moist ground. On contact with a passing snail, the latter is infested percutaneously or orally and the larvae moult inside the snail tissue to second- and third-stage larvae remaining one inside the other. Rats are infected by feeding on infested snails. After transentero-somatic invasion with passage into the brain, the juvenile adults arrive finally in the lungs, where they settle and propagate by eggs via the intestine. Man may be attacked by contaminated vegetables, infested snails or decapode crustaceans, which are paratenic intermediate hosts, and may suffer meningoencephalitis. Pigs and cattle are non-specific definitive hosts. - Diplotriaena agelaia, a lungworm of birds is transmitted by the grasshopper Cannula pelucida as an intermediate host (fig. 8.10, page 310).The Trichinellidae pass two parasitic generations within one host. In the first enteral phase, the ingested invasive larvae initially experience temporary host tissue contact and moult within the mucosa. They develop into adults that return to the lumen of the small intestine, copulate and propagate as viviparous intestinal trichinas. Thereafter, the expulsion of the adults closes the enteral phase. The delivered larvae immediately continue the cycle by an entero-somatic migration in order to reach the muscle tissues. After entering a muscle cell, the larvae open the second intracellular phase as muscle trichinas. As such, the larvae remain in diapause, which can last as long as the life of the host. The host or its carcass is usually eaten by carnivores. Trichinella spiralis: three phases are observed during the conversion of the contractile substance of the muscle cell to a trichina capsule after an initial hydropic swelling (fig. 3.7, page 190): first, a dedifferentiation (myofilaments break down), followed by a transformation (nuclei enlarge, Golgi-complexes appear, mitochondria divide) and, finally, a structuration (development of the capsule wall and the matrix in which the larva is embedded). The larva steers the processes by parakines produced by its stichosoma.

In Europe, Trichinella spiralis exhibit domestic cycles (domestic pigs) and separate silvatic cycles (fox, badger) with carnivorous ground-beetles as transport hosts. In the tropics, the aggressive hyena plays an important role among the large beasts of prey. Wild boar and warthog carry T. nelsoni, a species less pathogenic for man. In the Arctic, polar bear, wolves and walrus (also attacks seals) are important hosts. Fish and crustaceans act as transporting hosts to seals.

Trichinella pseudospiralis does not produce a capsule in muscles. It lives in birds and mammals; its larvae lie free in the sarcoplasma and in white fast and red slow contracting fibers. T. spiralis prefers red myoglobin-rich fibers.
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