Living in the Gut
For gastrointestinal nematodes, the most popular route of host entry is
through ingestion with food or water. After infection, these nematodes
tend to travel passively along with the flow of food in the gut to get to their
sites. The second route most typically begins with penetration of the skin
by infective larvae (as in hookworms) and requires an obligate migration
through the host to arrive at the gut. The infecting larvae migrate to the
lungs, where they are coughed up and swallowed, and thus they also enter
the gut orally and travel passively to their sites. There is an odd variation
(e.g.Strongylusspecies in horses) where the worms infect orally, migrate
around the body and then return to the gut where they began.Ascaris
lumbricoides, the giant roundworm that infects almost a billion humans,
provides a good example of this strategy. Orally infecting eggs hatch in the
small intestine and the larvae penetrate the gut wall and migrate to
the lungs, where they break through the alveoli and are coughed up and
swallowed. This ‘superfluous’ migration through the body can be very
costly, since most of the migrating worms are killed by the host’s immune
responses (Duncan, 1972; McCraw and Slocombe, 1976).
After arrival in the gut, there are two major obstacles to the successful
establishment and survival of intestinal nematodes: intestinal peristalsis
and the host immune response. Often the worms’ solutions to these two
problems are not mutually exclusive. For example, adultT. spiralishave
an intracellular habitat within the epithelial cells of the small intestine
(Despommieret al., 1978) and thus the worms are spared the expulsive
effects of intestinal peristalsis. However, this tissue habitat is readily
accessible to the host’s immune responses, and the worms are typically
expelled within 7–9 days after infection (Larsh and Race, 1954; Sukhdeo
and Meerovitch, 1977). The ovoviviparous females are able to produce all
of their progeny in this short time, and their tissue habitat makes it easy to
disperse the larvae into blood-vessels, from where they are passively
transported to the musculature (Sukhdeo and Meerovitch, 1980).
In contrast,H. polygyrus, which lives in the lumen of the small
intestine, may survive for 10–12 months in the gut. The host still mounts
an immune response to these worms, but it is much less severe and not
sterilizing (Urbanet al., 2000). In vertebrate hosts, more than half of the
humoral immune responses are concentrated in the gut to control the
intestine’s bacterial flora (Roitt, 1977), so few worms can fully escape
them, regardless of the habitat they choose. A highly detailed under-
standing of the complex nature of immune responses to these worms is
available (see Callardet al., 1996; Lenschowet al., 1996; Ekkenset al.,
2000; Urbanet al., 2000), but this topic is beyond the scope of this chapter.
However, it appears that successful parasites are frequently invisible to
their host’s immune responses.
Lumen-dwelling nematodes may escape the brunt of the immune
response, but they must deal with the inexorable expulsive effects
of peristalsis. Several holdfast mechanisms have evolved to deal with226 M.V.K. Sukhdeoet al.