CHAPTER 6 As most nematode roundworms are tiny and unpretentious, they escape public attention and are generally ignored by wild-life filmmakers. Nevertheless, they are one of the most numerous and diverse metazoan life-forms on this planet. The great majority are free-living, with species adapted to virtually every habitable aquatic or terrestrial ecological niche. A small minority are parasitic on plants and an even smaller proportion exploit animals for part or all of their life-cycle. Even so, the number of animal parasitic nematodes can be daunting for the student. Luckily, a detailed knowledge of every pathogenic species is unnecessary. This is because closely related nematodes tend to have similar life-cycles, epidemiology, pathogenesis and drug susceptibilities. An appreciation of group characteristics therefore saves a lot of repetitive learning. In this context, the best taxonomic level for our consideration is the superfamily (with names ending in –oidea; see Section 1.2.2). This chapter and the next provide an overview of these shared traits and outline the biology of an illustrative selection of important nematode parasites within each category. Nematodes are unique in the animal world as the fluid in their body-cavity is maintained at a relatively high pressure. Movement is governed by muscle bundles working against this inner hydrostatic tension and the elasticity of the tough outer layers of the body (the ‘cuticle’). These internal forces make swallowing difficult and so a large muscular pharynx (oesophagus) is needed to pump food into the intestine. All these functions are synchronised by a nerve ring around the pharynx which is connected via longitudinal nerves to various ganglia. Many anthelmintic drugs work by disrupting neuromuscular coordination, thereby rendering the worm incapable of feeding or maintaining its position within the host. Although apparently featureless at first sight (see Figure 6.1), many nematodes are easily identified when placed under the microscope. Memorising the diagnostic characteristics of every species would be a pointless exercise since descriptions and identification keys are readily available. However, the useful employment of such aides is dependent on an ability to recognise a few basic morphological features. Figure 6.1 Nematodes: gross appearance (Dirofilaria immitis from the pulmonary artery of a dog). Reproduced with permission of L. Venco. The cuticle which covers the surface of a nematode is not a featureless membrane but a complex structure with microscopic landmarks such as small pits containing tiny finger-like sensory organs (sensory papillae). More prominent diagnostic features are sometimes present, e.g. wing-like protrusions (‘alae’) and cuticular swellings that encompass the whole circumference of the body (see Figure 6.2 and Figure 6.3). Figure 6.2 Head-end of a nematode with cervical alae. (SEM of Passalurus, a nematode of rabbits and hares.) From Gibbons, 1986 with permission of CAB International. Figure 6.3 Head-end of a nematode (Oesophagostomum): a – leaf crown; b – buccal capsule; c – oral collar; d – cervical inflation; e – oesophagus. The position of a diagnostic feature along the body is often indicated by an appropriate descriptive word, for example: Nematodes have separate sexes. The posterior end of the female worm tapers to a blunt point, which is rarely of diagnostic value (see Figure 6.4). The male tail, in contrast, often has accessory sexual structures useful for identification. Figure 6.4 The tail-end of a female nematode (Haemonchus). Spicules are rod-like structures that can be protruded from the cloaca of the male to assist with the transfer of sperm during mating (see Figure 6.5). As they are made of chitin they show up well in prepared specimens under the microscope. They are usually paired and their shape and size is often diagnostic. Figure 6.5 Tail-end of a nonbursate nematode (Toxocara) showing one spicule protruding from the cloaca. The bursa (see Figure 6.6) is a very distinctive clasping organ situated at the posterior end of male worms belonging to particular superfamilies. The presence or absence of a male bursa enables a distinction to be made between ‘bursate’ and ‘nonbursate’ nematodes, which is a useful first step in worm identification. In some species the bursa is big enough to be seen with the naked eye, appearing as a terminal globule. It is formed of large expansions of the body wall within which are finger-like projections (‘bursal rays’) that have a sensory function. Figure 6.6 Tail-end of a male bursate nematode (Haemonchus) illustrating the bursa: a – bursal rays; b – spicules. The bursa is used to hold the female during mating (see Figure 6.7). This process is aided in some species by the excretion of a cementing substance which can sometimes be seen as a brown ‘blob’ on female worms. Unfortunately, this is of no diagnostic value. Figure 6.7 Male bursate worm (to right) using its bursa to clasp a female (diagonal). Nonbursate males achieve a mating posture by using sensory papillae near their cloaca for accurate alignment. Some are helped in this process by the presence of caudal alae which function like a miniature bursa. Many nematode species have a simple head with a small mouth, which provides little diagnostic assistance, but others have useful distinguishing features (see Figure 6.8), including: Figure 6.8 Head of a nematode (Strongylus vulgaris) showing: a – leaf crown; b – two teeth in buccal cavity. The mouth leads, directly or via the buccal cavity, to the muscular pharynx. This is a prominent internal feature when nematodes are viewed under the microscope. The basic form, seen in most free-living and plant parasitic nematodes, is known as a ‘rhabditiform oesophagus’ and has two thickenings along its length separated by a distinct constriction (see Figure 6.9). This form also occurs in preparasitic life-cycle stages of many animal nematodes. Figure 6.9 Pharynx of a free-living nematode. Photograph reproduced with permission of L.F. Khalil. In contrast, the parasitic stages of animal nematodes need to employ highly specialised feeding techniques and so the shape of the pharynx differs between groups. This can sometimes provide extra information to assist in the identification process. Practical tip box 6.1 When a tissue sample taken at necropsy or by biopsy is sectioned for microscopic examination, it is almost inevitable that any nematode contained therein will be cut transversely or obliquely. It is very unlikely, therefore, that any resemblance of a worm-like shape will be retained. Nevertheless, a nematode in section can be recognised as it is surrounded by a cuticle and the internal organs are often distinctive. The detailed appearance will, of course, vary depending where, along the length of the worm, the cut has been made. A typical example is displayed in Figure 6.10. Figure 6.10 Transverse section through a female nematode (Spirocerca) in a tissue section: a – cuticle; b – uteri filled with eggs; c – intestine. Photograph reproduced with permission of R.C. Krecek and K. Snowden. Many gastrointestinal nematodes, particularly those with small mouths, are found closely applied to the mucosal surface where oxygen tension is highest. Some swallow part-digested alimentary contents, but most feed on host secretions and may even stimulate the host to provide an abundant supply of modified mucus for them. Some may take in desquamated epithelial cells while others actively graze on mucosal lining cells. Plug feeders are more aggressive. They suck a mouthful of mucosa into their buccal cavity (see Figure 6.11). Teeth and enzymes reduce host tissue to a pulp which is swallowed. The worm then releases its grip and moves to a fresh site to repeat the process, leaving behind a small bleeding ulcer. Still more vicious are the species that bury their heads deep into the mucosa so they can suck arterial blood. Figure 6.11 Histological section of intestinal mucosa with a plug feeding nematode: a – buccal cavity; b – teeth; c – mucosal plug. Photograph from Jacobs, 1986. Reproduced with permission of Elsevier. Thus, there is a range of feeding mechanisms each provoking a different type of pathogenicity. This complexity is increased still further as nematodes also produce excretory and secretory (ES) substances, sometimes in copious quantities, which may be pharmacologically active or which may have immunogenic or immunomodulatory properties. The basic nematode life-cycle is very straightforward (see Figure 6.12), although many variations on this simple theme will become apparent as this chapter and the next unfold. Typically, parasitic females produce eggs that pass out of the host, usually in faeces. There follows a succession of four larval stages. These are conveniently called the first-stage larva, second-stage larva and so on, or alternatively: the L1, L2, etc. The stage that hatches out of the egg and the stage that is infective for the next host vary between nematode groups. Each larval stage develops until it outgrows its cuticle which is then discarded. This process is called ‘moulting’. When it emerges from its final moult, the nematode is an immature adult, either male or female. After a maturation period, mating occurs and egg-laying commences. Figure 6.12 Nematode life-cycle stages: E – egg; L1 – first-stage larvae; m – moult; L2 – second-stage larva; etc.; A – adult. Larvae redrawn after Stewart, 1954, with permission of Allen Press Publishing Services. The whole progression can be summarised as follows: Note that asexual multiplication does not take place during larval phases (in contrast to digenean trematodes, for example). So, each nematode egg has the potential to produce just one adult worm. Nematode eggs vary greatly in appearance and so are useful for diagnosing parasitic infections as they can easily be detected and counted in faecal samples (see Section 1.5.1). Practical tip box 6.2 Figure 6.13 Overview of the bursate nematode superfamilies. (*The taxonomic position of Dictyocaulus is unclear but is included here as it occurs in the lungs.) Figure 6.14 Strongyle egg surrounded by faecal debris including a pollen grain (below left). As noted earlier in this chapter, animal parasitic nematodes are divided into two major groups: bursate and nonbursate nematodes. When identifying parasitic nematodes, therefore, the first step is to look at the tail-end of the male worms. The presence of a bursa (see Figure 6.6) will narrow the choice down to the bursate superfamilies. There are four bursate nematode superfamilies (see Figure 6.13). Three of these, the Trichostrongyloidea, Strongyloidea and the Ancylostomatoidea (hookworms) are closely related, and are known collectively as ‘the strongyles’ (or ‘strongylate worms’ in some texts). They are predominantly gastrointestinal parasites with direct life-cycles. Members of the fourth bursate superfamily, the Metastrongyloidea, are associated with the respiratory tract and typically utilise an intermediate host in their life-cycle. The colloquial term ‘strongyle’ has no zoological validity but is very useful in Veterinary Parasitology since trichostrongyloid, strongyloid and hookworm species have much in common with respect to their biology, epidemiology and pathogenicity and because they are associated with an important animal welfare problem: parasitic gastroenteritis (PGE). Also, their eggs (with a few exceptions) are indistinguishable and so laboratory diagnostic reports will often report the number of ‘strongyle eggs per gram faeces’. A ‘typical strongyle egg’ is approximately 80 μm long, oval, thin shelled and generally contains 4–16 cells when passed in faeces (see Figure 6.14). The life-cycles of the strongyle worms have many similarities and follow the general pattern shown in Figure 6.15: The L1 develops within the egg and hatches. It feeds on bacteria, moults and sheds the cast-off cuticle to become an L2. The L2 also feeds on bacteria and moults to become the L3, but this time the shed skin is retained as a protective envelope (see Figure 6.16). It is now called an ‘ensheathed third-stage larva’ (see Figure 6.17). Figure 6.15 General strongyle life-cycle: a – eggs voided in faeces; b – L1 hatch and develop to L3; c – ensheathed L3 climb grass; d – L3 ingested by host; e – larvae travel to predilection site and develop to adults (details in text which uses the same lettering as shown above). Larvae after Eckert et al., 2008 with permission of Enke Verlag. Figure 6.16 Head-end of an ensheathed third stage strongyle larva showing the anterior part of the L3 within the retained L2 cuticle. Reproduced with permission of M.J. Walker. Figure 6.17 Ensheathed third stage strongyle larvae (Ostertagia): the L3 tail can be seen within the retained L2 cuticle of some larvae (bottom left); note the characteristic ‘crinkling’ of the sheath where it bends. Some strongyles have added extra steps to this basic pattern. For example, some can enter the host by skin penetration as well as by ingestion and some migrate through body tissues before settling in their predilection site. Where clinically relevant, these variations will be described in the text dealing with individual worms or groups. The condition most commonly associated with strongyle worms is parasitic gastroenteritis, characterised by diarrhoea and weight-loss or suboptimal weight-gains (see Section 8.2.1). PGE is a seasonal disease driven by climatic factors. Ambient temperature is the dominant force in temperate regions, while rainfall patterns are of greater significance in the tropics. Strongyle eggs and larvae will not develop at temperatures below about 8–10°C but, above this threshold, growth and development accelerate with increasing warmth. The ensheathed third-stage larvae, which are entirely dependent on stored glycogen, become more active at higher temperatures and use up their energy reserves more quickly. Thus, warmer conditions encourage infective L3 to accumulate more quickly but also shorten their life-span. Consequently, the disease risk for susceptible animals grazing contaminated pasture depends on a balance between: This dynamic determines the overall density of third-stage larvae on the herbage (measured as L3/kg dry matter) which, in turn, governs the level of exposure of grazing animals to parasitism (since their daily dry matter intake is fairly constant for a given age, weight and class of livestock). The preparasitic life-cycle functions most efficiently in humid conditions. The L3 is the most robust larval stage (presumably because the retained sheath provides protection), but it will nevertheless succumb to desiccation or extreme temperatures. Dung pats and snow cover both provide insulation against adverse conditions. Since levels of pasture contamination are determined by climate, they follow an annual pattern typical for each locality, although this stereotype can be modified by short-term weather anomalies (e.g. an unusually cold spring or a summer drought). The precise timing of events is also influenced by the composition of the strongyle population as there are subtle differences in threshold temperatures and rates of development between species (Trichostrongylus tends to peak later than Teladorsagia, for example). An example of the seasonal fluctuation that typically occurs in the number of L3 per kg grass on a permanent calf pasture in a temperate climate is depicted in Figure 6.18: Figure 6.18 Epidemiology of parasitic gastroenteritis (PGE) in the northern hemisphere: numbers of infective third stage larvae on pasture throughout year: a – overwintering L3; b – L3 die in spring; c – eggs hatching but larvae not yet at L3 stage; d – new L3 accumulating (‘autoinfection peak’); e – new recruits outnumbered by dying L3; f – overwintering survivors (details in text). Temperature is not a limiting factor in warmer regions. Strongyle eggs and larvae, like those of most other nematodes, need a humid microclimate in which to survive. During the dry season, viable infective larvae are mostly confined to faecal deposits as any L3 on herbage are likely to become desiccated. The onset of rain releases large numbers of L3 onto pasture. Larval development and translation continue throughout the wet season increasing disease risk still further. Once the L3 has infected a susceptible host, it finds itself in a consistently warm environment with an abundant food supply and so the parasitic phase of the life-cycle can proceed without interruption. If this provokes clinical signs, the process is termed ‘Type I’ disease. Many strongyle and other nematode species are capable of pausing parasitic development for a period of weeks (or in some cases many months). This phenomenon is known variously as ‘arrested’ or ‘inhibited’ development, or ‘hypobiosis’. It is a mechanism for optimising chances of survival for the next generation by synchronising the parasitic life-cycle with external events. In the tropics, for example, parasitic larvae of some species may develop normally within their host during the wetter months but may undergo arrested development during the dry season. In this way, developing worms will not attain maturity and start laying eggs until the humidity of the external environment is favourable for the survival of their off-spring. Similarly, in temperate regions, worms may overwinter in a hypobiotic state to delay egg-production during the cold season. Arrested development is genetically based and there may be strain variation within a species, so populations may behave differently in different localities. The mechanism may be switched on while the L3 is still on pasture (e.g. cold autumnal nights influencing Ostertagia larvae in Scotland), although in most cases the trigger factor is still unknown. Arrested larvae can accumulate in host tissues over time but, in some cases, may ‘wake up’ almost simultaneously. If large numbers of larvae emerge from the alimentary mucosa together, the damage they cause can be extensive. This is known as ‘Type II’ disease. Help box 6.1 Cattle and sheep are able to develop protective immunity against many strongyle parasites, although this generally occurs only after prolonged exposure. Consequently, calves and lambs remain vulnerable throughout their first grazing season but disease is relatively uncommon later in life. Goats, on the other hand, remain susceptible throughout their lives. Horses occupy an intermediate position on this scale. The epidemiology of PGE in sheep has an extra component as the immunity of breeding ewes to gastrointestinal nematodes declines significantly over a period of several weeks starting shortly before lambing. During this time, known as the ‘periparturient relaxation of immunity’, patent trichostrongyloid infections are able to establish. As a result, faecal egg-output increases enormously (see Figure 6.19). The mechanism for this ‘periparturient egg-rise’ is unclear but it could be associated with the diversion of IgA (which is normally secreted with gastrointestinal mucus) to the udder for colostrum production. Figure 6.19 The faecal output of strongyle eggs by ewes around lambing time (the ‘periparturient egg-rise’). Help box 6.2
Nematoda (‘roundworms’) part 1: concepts and bursate nematodes
6.1 Introduction
6.2 Key concepts
6.2.1 Recognition features
Surface structures
Accessory sexual structures
Spicules
Bursa
Head, mouth and associated structures
Appearance in histological sections
6.2.2 General biology
Feeding mechanisms
Life-cycle
6.3 Bursate nematodes
6.3.1 Bursate superfamilies
The ‘strongyles’
General strongyle life-cycle
General strongyle epidemiology
In temperate climates
In tropical climates
Type I and Type II disease
Immunity
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