INTESTINAL WORMS

Intestinal helminths

Whats new ?
An increasing number of large-scale helminth control
programmes are being planned

Michael Brown

Single-dose treatment with albendazole is a safe and

effective therapy for hookworm and Ascaris infections;
albendazole is probably safe in pregnancy
Ivermectin is an effective and well-tolerated therapy for
Strongyloides infection
Increasing attention is being paid to the effect of
co-infection with helminths on other diseases such as
malaria, tuberculosis, HIV and asthma

Intestinal helminths (Figure 1) are common in the developing

world; current estimates suggest that one-third of the worlds
population is infected. Although most infections are light and
asymptomatic, they are a significant cause of morbidity in heavily
infected individuals and there is evidence that even moderate infections may have profound effects on pregnancy outcome, growth
and cognitive function.

Many helminths exhibit a highly over-dispersed distribution of

worm numbers; that is, most infected individuals harbour a few
parasites, but a few have heavy burdens. Many factors (social,
behavioural and genetic) determine which individuals within a
community carry the heaviest infections. Ageintensity relationships vary between species; there is an increase in hookworm
intensity with age, but a peak intensity in childhood for Ascaris
and Trichuris infections.
The total burden of disease caused by helminth infections has
been estimated using worm-burden thresholds:
above the lower threshold, there are detrimental effects on
physical fitness and school performance
above the higher threshold, there is a risk of clinically overt
illness.
These estimates have been used to guide world and national policies for helminth eradication.1 Public health education and provision of better sanitation (Figure 2) are important components, but
the availability of safe and effective antihelminthic drugs makes
mass treatment of communities in endemic regions the primary
control strategy.

for eosinophil proliferation and activation has been described

within the framework of the type 1/type 2 model. Research has
established the existence of a dichotomous specific immune
response to infection mediated by different subpopulations of
T helper lymphocytes. Type 1 helper (Th1) lymphocytes secrete
cytokines such as interleukin-2 (IL-2) and interferon-, and stimulate type 1 immunity, which is characterized by phagocytosis and
intracellular killing of microbes. Most micro-organisms (particularly intracellular bacteria, protozoa and viruses) tend to stimulate
a type 1 response, which is essential for effective immunity against
these organisms. However, large eukaryotic pathogens (particularly
helminths) tend to induce a type 2 immune response, which is
characterized by B cell proliferation and antibody and eosinophil
production, and is mediated by Th2 cells, which secrete IL-4, IL-5,
IL-10 and IL-13.
Interactions with other infections and allergy Th1 and Th2
cells cross-regulate each other, and this has generated a hypothesis
that co-infection with helminths may subvert the immune response
to pathogens such as HIV, tuberculosis and malaria.2,3 Related
mechanisms by which helminths might suppress the immune
response have been suggested as contributing factors in the
increasing prevalence of atopy and asthma in more industrialized
regions of the world where the prevalence of helminth infection
has been declining.4 The impact of mass treatment on allergy and
on co-infections has not been well studied.

Immunology

Hookworms

Understanding of how helminths have evolved mechanisms to

evade the immune system, in many cases harnessing it for their
own survival, is crucial to the development of vaccines and has
been the subject of intense study. Helminths use various strategies
to avoid recognition and expulsion by the host, but such infections
are characterized by a stereotypical host immune response.
Eosinophils and type 2 immunity eosinophils appear to
have evolved as the principal effector cell against helminth infection. The network of cellular and cytokine responses required

Life cycle two species of hookworm complete their life cycles

in humans Necator americanus and Ancylostoma duodenale.
Hookworm larvae in moist soil penetrate exposed skin, are carried
by the circulation to the lungs, penetrate the alveolar walls and
progress up the trachea, where they are swallowed and carried to
their final habitat in the small intestine. The adults attach themselves to the mucosa with their buccal cavities, and after 36 weeks
the females produce up to 30,000 eggs per day (depending on the
species), which are passed in the faeces. Adult hookworms live
for 19 years.
Clinical features the main burden of disease attributable
to hookworm infection results from iron-deficiency anaemia
(Figure 3) caused by blood loss from the site of attachment to the
mucosa. Whether by anaemia or by other mechanisms, childhood

Epidemiology

Michael Brown is Specialist Registrar in Infectious Diseases and General

Medicine at the Hospital for Tropical Diseases and University College
Hospital, London, UK. Conflicts of interest: none declared.

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Common intestinal helminths

Nematodes
(roundworms)

Hookworms
Cestodes
(tapeworms)

Organism
Trichuris trichiura
Enterobius vermicularis
Ascaris lumbricoides
Strongyloides stercoralis
Capillaria philippensis
Anisakis simplex
Ancylostoma duodenale
Necator americanus
Taenia saginata
Taenia solium
Diphyllobothrium latum

Mode of transmission
Ingestion of eggs
Ingestion of eggs
Ingestion of eggs
Skin penetration by larvae
Ingestion of raw fish
Ingestion of raw fish
Skin penetration by larvae
Skin penetration by larvae
Ingestion of undercooked beef
Ingestion of undercooked pork
Ingestion of freshwater fish

growth, school performance, pregnancy outcome and worker

productivity are affected. Several studies have shown the benefits
of deworming in childhood and pregnancy, particularly if this is
combined with increased iron intake, though the evidence for
important benefits on cognitive performance is debated.5
Diagnosis adult hookworms are about 1 cm long and can
be seen in the small intestine on endoscopy. The diagnosis is
normally made by visualization of hookworm eggs in the faeces
under light microscopy. Infection may be light, and at least three
stool specimens should be examined. Concentration methods
are more sensitive than direct smears and are commonly used in
hospital laboratories.
Management a single dose of albendazole, 400 mg, is well
tolerated and effective. Very heavy infections may require a second
dose. An alternative is mebendazole, 100200 mg b.d. for 3 days.
Both drugs are probably safe in pregnancy but best avoided in the
first trimester.
Cutaneous larva migrans various species of animal hookworm (e.g. A. braziliense, A. caninum) can infect humans who
are exposed to dog faeces, commonly on beaches in the Caribbean
(Figure 4). The larvae cannot penetrate the dermis, and migrate
through the epidermis leaving intensely pruritic, serpiginous tracks.
Ivermectin, 200 g/kg, or albendazole, 400 mg o.d. for 3 days, is
effective.

Ascaris lumbricoides
Life cycle embryonated eggs in moist soil are ingested and
hatch in the small intestine. The larvae penetrate the mucosa,
enter the blood and circulate to the alveolar capillaries, where
they burrow through to the respiratory tree, are carried up the
trachea and are swallowed for a second time; on reaching the small
intestine, adult females lay 200,000 eggs per day. The incubation
period from egg ingestion to egg-laying is 6070 days, and adults
live for up to 2 years.
Clinical features the migratory phase of infection with
A. lumbricoides (and, less commonly, hookworm, Strongyloides
and schistosomes) can cause Loefflers syndrome a self-limiting
illness with cough, fever, dyspnoea, wheeze and eosinophilia. More
serious complications of A. lumbricoides infection include biliary
and intestinal obstruction (Figure 5) and migration of worms to
other organs; these cause many deaths in developing countries.
However, the greatest burden of disease results from the nutritional
consequences of heavy worm loads in the small intestine. Several
clinical trials have shown improvements in nutritional status and
growth following deworming, even at low worm burdens.
Diagnosis Ascaris eggs are detected by stool microscopy and
are usually present in large numbers. The adult worms are about
1535 cm in length and may be passed in the stool, particularly

3 Severe hookworm anaemia.

This young Thai woman
presented with fatigue and
dyspnoea. Her haemoglobin
concentration was 2.2 g/dl.
Stool microscopy revealed a
heavy hookworm infection.

2 Moist soil provides an ideal environment for the maturation of

hookworm and Strongyloides larvae, deposited when toilets and
latrines are unavailable. Ascaris and Trichuris eggs can survive in drier
conditions and are more widespread.

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individuals, may be followed by significant improvements in school

performance.
Diagnosis adults attached to the intestinal mucosa are seen on
colonoscopy or on a prolapsed rectocele. The eggs can be detected
on stool microscopy.
Management mebendazole, 100 mg b.d. for 3 days, or
albendazole, 400 mg o.d. for 3 days, is reasonably effective. Cure
rates are lower than in hookworm and Ascaris infections, and
treatment may need to be repeated.

4 Cutaneous larva
migrans. This man
walked barefoot on a
beach in the Caribbean.
Over the next few days,
he developed intensely
itchy, serpiginous
eruptions on his toes.
Infective larvae of
animal hookworms can
invade the skin but not
penetrate the dermis,
and migrate through the
epidermis leaving typical
tracks.

Strongyloides stercoralis
Life cycle the life cycle is complex. Filariform larvae in the
soil penetrate exposed skin, pass via the blood stream to the lungs,
break into the alveolar spaces, ascend the trachea and are swallowed to reach their final habitat in the small intestine, where the
adults develop. Females produce eggs that hatch in the mucosa,
and the larvae bore through the epithelium into the faeces. At this
stage, larvae can develop into free-living adults, which continue
their life cycle indefinitely in the soil, or into filariform larvae,
directly via three moults. Filariform larvae are usually passed in
the faeces, but may re-invade the host in the lower gastrointestinal
tract or perianal skin before evacuation. Because of this process of
autoinfection, S. stercoralis is one of the few species of helminth
that can complete its life cycle and thereby multiply in humans.
Clinical features many infected individuals are asymptomatic, and ongoing, low-level autoinfection means that they may
harbour infection for decades after leaving endemic areas. Larva
currens (a creeping, pruritic eruption on the skin) and eosinophilic
pneumonia are occasional manifestations. Subsequent immunosuppression caused by corticosteroids, haematological malignancy
or retroviral infections (particularly HTLV-1) may lead to a severe,
disseminated hyperinfection syndrome characterized by colitis,
haemorrhagic pneumonia (Figure 7) and Gram-negative sepsis.
Diagnosis larvae can be visualized on stool microscopy; culture techniques may improve the diagnostic yield. Serology is more
sensitive. In disseminated infection, larvae are found elsewhere
(e.g. sputum, in tissue biopsies).

after antihelminthic treatment. Occasionally, they migrate back up

the gastrointestinal tract and appear through the mouth or nose.
Management albendazole, 400 mg, is effective, as is mebendazole, 100 mg b.d. for 3 days. Levamisole and piperazine are less
well tolerated.

Trichuris trichiura
Life cycle embryonated eggs in moist soil are ingested, hatch
in the small intestine and invade the mucosa; here, they develop for
1 week before re-entering the lumen and travelling to the caecum,
where they invade and attach themselves within the superficial
mucosa. Females produce up to 20,000 eggs per day and survive
for up to 1 year.
Clinical features most infections are light, but heavy infections cause haemorrhage, dysentery, rectal prolapse (Figure 6) and
an acute-phase response, which may contribute to reduced iron
status and poor growth. Treatment, even of less heavily infected

5 Ascaris causing
bowel obstruction. The
intestinal volvulus and
obstruction caused
by this large bolus of
A. lumbricoides worms
in the stomach led to
the death of a 2-year-old
child.

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6 Trichuris rectal prolapse. This child had a chronic history of bloody

diarrhoea and failure to thrive. The characteristic T. trichiura adults, with
whip-like anterior ends buried in the mucosa, are seen attached to this
prolapsed rectum.

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in the small intestine or ingestion of eggs via the faeco-oral route

leads to cysticercosis (see page 70).
Clinical features tapeworm infections are largely asymptomatic apart from the distress caused by passage of the motile
proglottides. The clinical features of cysticercosis are discussed on
page 71.
Diagnosis T. solium and T. saginata proglottides can be seen
with the naked eye and differentiated under the microscope.
Management praziquantel, 10 mg/kg, is effective. Niclosamide
is also effective, but has more side-effects. Patients should be
warned that treatment may lead to passage of the entire worm.
Previously, purgatives were also given, with the aim of aiding
passage of the worm and preventing autoinfection from release of
T. solium eggs in the intestine. This risk is probably unfounded,
however, and the advice is probably no longer necessary.

Management albendazole, 400 mg b.d. for 3 days, is reasonably effective in chronic infections and is better tolerated than
thiabendazole, 25 mg/kg b.d. for 3 days. Currently, the treatment
of choice is ivermectin, 200 g/kg daily for 2 days, and this is particularly helpful in patients with disseminated infection; prolonged
courses of treatment may be necessary.

Enterobius vermicularis
Life cycle E. vermicularis is the only gastrointestinal helminth
that remains widely distributed in temperate climates. Swallowed
eggs hatch in the duodenum and the larvae pass to the caecum,
where they mature. The females, which are about 1 cm long, lay
10,00015,000 eggs after emerging in the perianal region. The eggs
are immediately infectious and therefore do not require a period of
maturation in the environment. Children often infect themselves
from eggs under their fingernails.
Clinical features as the females die, they cause intense pruritus ani. Often, all members of a household are affected.
Diagnosis eggs are most easily identified by direct microscopy
of adhesive tape that has been briefly pressed against the childs
perianal skin.
Management mebendazole, 100 mg repeated after 2 weeks, is
effective. All members of the family should be treated, and hygiene
measures to break the autoinfection cycle are required.

REFERENCES
1 Prevention and control of schistosomiasis and soil-transmitted
helminthiasis. World Health Organ Tech Rep Ser 2002; 912: i-57.
2 Fincham J E, Markus M B, Adams V J. Could control of soil-transmitted
helminthic infection influence the HIV/AIDS pandemic? Acta Trop
2003; 86: 31533.
3 Bentwich Z. Good worms or bad worms: do worm infections affect the
epidemiological patterns of other diseases? Parasitol Today 2000;
16: 312.
4 Yazdanbakhsh M, Kremsner P G, van Ree R. Allergy, parasites, and
the hygiene hypothesis. Science 2002; 296: 4904.
5 Dickson R, Awasthi S, Williamson P et al. Effects of treatment for
intestinal helminth infection on growth and cognitive performance
in children: systematic review of randomised trials. BMJ 2000; 320:
1697701.

Tapeworms
Life cycle the life cycles of the pork tapeworm (Taenia
solium) and the beef tapeworm (T. saginata) are similar in most
respects. Humans are the definitive hosts; the adult lives in the
small intestine, reaching 28 m in length. Segments containing
thousands of eggs (proglottides) are passed in the faeces. When
ingested by pigs (T. solium) or cows (T. saginata), the eggs hatch,
releasing a larval form that migrates into, and encysts in, striated
muscle. Inadequately cooked infected meat can infect humans,
completing the life cycle. In the case of T. solium, autoinfection

FURTHER READING
Awasthi S, Bundy D A P, Savioli L. Helminthic infections. BMJ 2003; 327:
4313.
(Brief summary of the evidence supporting a worldwide policy for
control of these infections, and of the organizations involved in its
implementation.)
Cook G C, Zumla A. Mansons tropical diseases. 21st ed. Oxford: Elsevier,
2003.
(Standard text, with clear life cycle diagrams; covers less common
intestinal helminths not discussed in this contribution.)
Roitt I, Delves P. Roitts essential immunology. 10th ed. Oxford: Blackwell
Science, 2001.
(Standard immunology text, covering the immune response to
helminth infection.)
Savioli L, Crompton D W T, Neira M. Use of antihelminthic drugs during
pregnancy. Am J Obstet Gynecol 2003; 188: 56.
(Summary of the evidence supporting use of albendazole,
mebendazole and praziquantel in pregnancy.)

Acknowledgement

7 Disseminated Strongyloides lung histology. This patient with

leukaemia developed fatal disseminated S. stercoralis infection. In
the lungs, this caused haemorrhagic pneumonia. Filarifom larvae and
inflammatory infiltration with RBCs and eosinophils are seen within an
alveolus at post-mortem.

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Figures 27 are reprinted from Peters W, Pasvol G. Tropical

medicine and parasitology. 5th ed. Philadelphia: Mosby, 2002
with permission from Elsevier. 2002 Mosby

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