Parasitic phase of life-cycle:

3. Infective L₃ can enter the host by skin penetration. If entering an adult mare in this way, the larvae accumulate in subcutaneous tissues and migrate to the mammary gland during lactation.
   
4. Larvae are acquired by foals either by skin penetration or from the mare via colostrum and milk. They travel to the small intestine where they develop into females that are able to lay fertile eggs even though no males are present in the parasitic phase of the life-cycle (i.e. they are parthenogenic).
   
5. Larvated eggs are voided with faeces bringing us back to (a).

(In some species, e.g. S. stercoralis in dogs, the egg hatches in the intestine and the L₁ is passed in faeces.)

Free-living phase of life-cycle

6. All hatched larvae that are not predestined to become parasitic females develop via a free- living L₄ stage to become free-living adult males and females.
   
7. The free-living females produce larvated eggs and, once again, we are back to (a).

Pathogenicity

Patent infections are commonest in very young animals and may be associated with diarrhoea or dysentery, particularly in piglets and puppies. Often, however, infections are symptomless even though faecal egg-counts are high.

Species such as S. stercoralis, with eggs that hatch before leaving the host, can give rise to persistent infections, especially if the animal is immunocompromised. In this case, larvae that develop to the infective stage within the host digestive tract penetrate the intestinal wall or perianal skin. This is known as ‘autoinfection’.

T. canis in paratenic hosts

In any warm-blooded animal that is not a dog, fox or other canid, T. canis eggs hatch and larvae migrate via the liver and heart to the lungs, as happens in the initial stages of hepatotracheal migration (see Figure 7.8). In the lungs, however, they stay in the blood-stream and are returned to the heart to be distributed around the whole body via the general circulation. They settle out in various somatic tissues and become arrested in their development (see Figure 7.10). They now wait for the paratenic host in which they reside to be eaten by a dog, fox, wolf, dingo, etc. If and when this happens, the larvae are released within the digestive tract of their new host and can resume their normal developmental behaviour.

The category ‘any warm-blooded animal that is not a dog, fox or other canid’ includes humans and somatic infections can establish in people just as in any other paratentic host. T. canis is therefore a potentially zoonotic pathogen (see Section 9.3.2).

T. canis in older dogs

When infection takes place in dogs older than about two months of age, only a very small proportion (if any) of T. canis larvae undergo hepatotracheal migration. Most become somatic larvae in the same way they would if they were in a paratenic host. In this case, however, they are waiting for a reactivation stimulus. This happens only after the host becomes pregnant. The greatest numbers of somatic larvae are activated in late pregnancy, some during lactation, but others remain dormant until subsequent pregnancies. Activated larvae migrate to the placenta or mammary glands and are thereby transferred to foetuses in utero (‘transplacental transmission’) or to neonates via colostrum or milk (‘transmammary transmission’). Once in the foetus or puppy, the larvae undergo hepatotracheal migration. The first adult worms reach maturity in the small intestine in the third week of independent life.

Ascaris suum

Each phase of the parasitic life-cycle can result in economic or welfare problems in pigs, including all the direct and indirect effects described in the ‘General pathogenicity’ section above. Even small numbers of A. suum larvae passing through the liver can trigger a fibroblastic response (see Figure 7.11). The lesions are roughly spherical, except where they meet the liver surface, and they sometimes have a haemorrhagic centre. They vary from several millimetres to a couple of centimetres in diameter with white strands radiating out between adjacent liver lobules. The pathological term for these ‘milk-spots’ is ‘chronic focal interstitial hepatitis’. The lesions resolve in about six weeks leaving a very small nodule.

There is a complex relationship between immunity and ‘milk-spots’. On exposure to A. suum, pigs develop a protective immunity over a period of months. Initially, migrating larvae pass through the liver and lungs, and it is not until they arrive back in the intestine that they succumb to immune attack. Thus, it is not an unusual occurrence in an abattoir to find ‘milk-spots’ in the livers of younger pigs even though they have no adult worms in the intestine. As pigs become more solidly immune, larvae are killed before they reach the liver, and ‘milk-spots’ are therefore observed less frequently in slaughtered sows.

Sows nevertheless play an important role in the epidemiology of ‘milk-spot’ livers. Despite their immunity, a small proportion of sows do carry a small number of adult worms in their alimentary tract. As female A. suum are such prolific egg-layers, the farrowing house can quickly become contaminated. As a result, the susceptible piglets acquire infection, carry it with them to the fattening house and perpetuate the problem.

Parascaris equorum

As adult horses rarely harbour patent infection, the transmission of P. equorum is generally from one year’s foals to the next via contaminated pastures. Foals are often infected in their first month of life but eggs do not appear in the faeces for a further 10–12 weeks (i.e. the prepatent period). Light infestations are asymptomatic but perpetuate the transmission cycle by contaminating the pasture anew. In heavier infections, lung damage by migrating larvae may provoke coughing and nasal discharge, while intestinal worms contribute to unthriftiness or weight-loss. As the worms are so large, obstructive impaction or even perforation of the small intestine can occur in extreme cases with severe or fatal consequences.

Toxocara canis

If left untreated, almost all puppies will harbour T. canis to a greater or lesser extent. Most of the worms are acquired prenatally, but these are later supplemented by the ingestion of larvae passed with colostrum and milk. Further infection can take place by swallowing embryonated eggs from the environment. Feral canids are exposed to yet another source of infection once they start to take solid food – somatic larvae in the tissues of prey animals such as mice.

The prepatent period of T. canis is 4–5 weeks, but eggs start to appear in the faeces of puppies after the second week of life. This apparent anomaly occurs because activation of somatic larvae in the bitch happens during the last three weeks of gestation. Prenatally acquired larvae have therefore started their hepatotracheal migration in the pups prior to whelping. Infected pups excrete (literally) millions of T. canis eggs in their faeces during the suckling period.

Help box 7.2

From the age of about six weeks, pups start to lose their intestinal T. canis population spontaneously, a phenomenon well-known to all dog breeders (see Figure 9.20). During this period, a progressively greater proportion of ingested larvae become arrested in somatic tissues rather than taking the hepatotracheal route. Thus, only a minority of dogs over 4–6 months of age harbour patent infection and they are likely to have no more than a few adult worms. Their T. canis egg-output is correspondingly low but sufficient nonetheless to ensure widespread environmental contamination. Higher egg-counts are, however, encountered in suckling bitches as these often experience a temporary increase in their intestinal worm burden. Adult foxes, too, tend to carry greater numbers of intestinal T. canis than most domestic dogs.

As with many other ascarid infections, a few worms do no discernible harm, but greater numbers can stunt growth and cause serious, and sometimes fatal, disease (see Section 9.2.1).

Toxocara cati

T. cati infects cats and other felidae. Its biology is in many respects similar to that of T. canis but there are only three routes of transmission – transmammary, embryonated eggs and infected paratenic hosts. As there is no prenatal infection, kittens are first infected during suckling and eggs will not appear until the end of the prepatent period (i.e. when the kittens are around 8 weeks old).

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