Volume 6. The
M. Arcari 1, A. Baxendine 1 and C. E. Bennett2
Diasys Ltd 2.
University of Southampton
Infections of the alimentary tract and associated organs-
Part One – The Trematodes
of the Alimentary Canal and asociated organs. Part One - The Trematodes
and Echinostoma species are
trematodes which parasitise the liver and intestines of a variety of
vertebrates. They are hermaphroditic and their distinguishing characteristics
are shown in Table 1.
hepatica trematodes are not thought to
infect man but in fact man is not an unusual host, with infections being
reported in many countries including Europe and the USA. The eating of
unwashed watercress appears to be the source of infection, with them ending up
in the liver. The most common host is sheep where they can cause severe
buski (giant intestinal fluke) is a
duodenal parasite infecting both man and pigs. They are found widespread in
Asia and China, but they have been found to be endemic in Taiwan, Thailand,
Bangladesh and India. Night soil is used as a fertiliser in these countries on
plants such as water chestnut and caltrops. The snails graze on these crops
and also the definitive hosts eat them raw and unwashed, peeling the edible
water plants with their teeth.
Infection with Echinostoma
species is thought to be contracted by injestion of fresh water snails
containing metacercaria. Such as Echinostoma
ilocannum which occurs in the Philippines. The metacercariae infect the
large snail Piola luzionica and in
return are eaten raw.
Despite the large numbers of these flukes they are
of little medical importance, the most important being F. buski.
of adult in host
130 - 150mm
63 - 90mm
160 – 190mm
70 - 90mm
130 – 140mm
80 - 85mm
88 – 116mm
58 - 69mm
describing the characteristics which differentiate the various Fasciola
species which are important to man.
Life cycle and transmission
The life cycles of Fasciola,
Fasciolopsis and Echinostoma species are complex, requiring more than one
intermediate host. (Fig. 2)
Adult worms inhabit the liver or bile ducts of the definitive host (human), where they lay many eggs which are deposited into the environmnent in the faeces. They are immature when passed. If they are passed into water they become mature in 9 to 15 days at the optimum temperature of 22 - 25°C.
2. The general life cycle of Fasciola, Fasciolopsis and
Echinostoma species. They all
involve one or more intermediate hosts.
The larvae (miracidia) develop within the eggs and
hatch out into water, where they then penetrate the snail (intermediate host).
The miracidia must find a snail within 8 hours of hatching out of the egg.
Each species of fluke favours one particular intermediate host; F. hepatica invade snails from the genus Lymnaea, the most important being Lymnaea truncatula and F.
buski invade snails of the family Planorbidae, e.g. Segmentina hemisphaerula.
Within the snails the miracidia mature into sporozoites and then into redia and cercariae. This development takes 1 to 2 months according to the temperature. (In summer there is only one redial generation but in cooler weather there are two redial generations.)
The cercariae leave the snail, usually at night: they then swim around for several hours and then encyst (forming a resistant external wall) on submerged vegetation or fresh water fish.
If the cysts are ingested by a definitive host, the metacercariae excyst in the duodenum. They then migrate through the intestinal wall and either reach the liver tissue and bile ducts via the body cavity or via the lymphatics and the circulation. They require 2 to 3 months to reach maturity.
The life cycle of the Echinostomes
differs by one minor point: the cercariae encyst wither within the tissues
of the same molluscan host in which sporocysts and rediae develop, or
penetrate and encyst in other animals such as amphibians or fish.
The morphology of the adult flukes of Fasciola, Fasciolopsis and Echinostoma
species is well documented. (Fig. 3)They
are large leaf-shaped parasites about 2 –3 cm long. There are two suckers, an anterior oral sucker surrounding
the mouth and a ventral sucker (acetabulum) on the ventral surface.
3. Adult fluke of a Fasciola
trematode. Their morphology shows a large leaf-shape about 2 – 3cm long
with two suckers, an oral and a ventral one.
The outer tegument is covered in tiny spines which
face backwards enabling them to attach themselves along with their suckers to
Ova are all thin shelled, ellipsoid, quinone
coloured (bile stained) with an operculum that is often inconspicuous. (Fig. 4 & 5) Although ova of Echinostoma species can usually be differentiated by size due these
flukes beign much smaller in size than F.
Buski and F. hepatica, there is
much cross-over in the size of Fasciola
and Fasciolopsis species as shown in
Light infections due to Fasciola
hepatica may be asymptomatic. However,
they may produce hepatic colic with coughing and vomiting; generalised
abdominal rigidity, headache and sweating, irregular fever, diarrhoea and
illustrating the morphology of a Fasciola
ova, the miracidium develops within the egg. (Drawn and adapted from Smyth,
Figure 5. Ova of Fasciola are ovoid in shape, quinone colour and often showing an inconspicuous operculum. Fasciola hepatica ova measure 130 - 150mm by 63 - 90mm. There is much cross-over in ova size between all of the Fasciola species.
Infections due to Fasciola
gigantica occur mainly in cattle
raising areas and cause clinical symptoms similar to those of Fasciola
hepatica although human infections are less common.
The adult flukes of Fasciolopsis
buski attach to the intestine,
resulting in local inflammation and ulceration. Heavier infections may subsequently lead to abdominal pain,
malabsorption and persistent diarrhoea, oedema and even intestinal
obstruction. Marked eosinophilia may be seen.
The adult flukes of Echinostoma
species attach to the intestine resulting in little damage to the intestinal
mucosa. Light infections are generally asymptomatic and heavy infections may
produce light ulceration, diarrhoea and abdominal pain.
of adult in host
Liver and bile ducts
Liver and bile ducts
26.5- 30mm by 15 – 17mm
26.5- 30mm by 15 – 17mm
26.7 by 15mm
38 – 45mm
by 22 – 30mm
Shape of ova
shoulders Bile stained
shoulders Bile stained
shoulders Bile stained
Dark brown, thick
shelled and large operculum
Eating raw or pickled
Eating raw or pickled
Eating raw fresh water
Eating infected ants
Malaise and right
upper quadrant pain
Biliary and digestive
Table 2. Table summarising the less common flukes that are
known to infect man.
westermanni is a lung fluke found in both
humans and animals. The adults
are 12mm long and are found in capsules in the lung.
Although they are hermaphroditic, it is necessary for worms to be
present in the cyst for fertilisation to occur. The disease is seen in the Far East, China, South Eat Asia
Humans become infected by ingestion of
insufficiently cooked crayfish or crabs containing metacecariae which excyst
in the intestine, penetrate through the wall into the peritoneal cavity and
make their way through the diaphragm and pleura into the lungs.
The lung cysts in which the worms most commonly
occur usually contain 1 – 3 flukes. The eggs become freed into the bronchial
tubes and pass out with sputum, but they may also appear in the faeces in
large numbers, as a result of being swallowed.
The adult worm is an ovoid, reddish brown fluke
about 12 mm long.
The eggs are ovoid, brownish yellow, thick shelled
and operculated. They measure 80
– 100mm by
45 - 65mm and
may be confused with the ova of Diphyllobothrium
latum. (Fig. 11)
11. Saline smear of Paragonimus
westermanni egg. The egg shells are thick and operculated, measuring
approximately 80 – 100mm by 45 - 65mm.
As the parasites grow in the lung cyst,
inflammatory reaction and fever occurs. The
cyst ruptures and a cough develops resulting in an increase in sputum.
The sputum is frequently blood tinged and may contain numerous dark
brown eggs and Charcot-Leyden crystals. Haemoptisis
may occur after paroxysms of coughing. Dyspnoea
and bronchitis develop with time. Bronchiectasis
may occur and pleural effusion is sometimes seen.
The disease resembles pulmonary tuberculosis. Cerebral calcification may also occur.
The Schistosomes are blood
trematodes belonging to the Phylum Platyhelmintha.
They differ from other trematodes in that they have separate sexes. The male
worms resemble a rolled leaf where they bear the longer and more slender
female in a ventral canal (the gynaecophoric canal). They require definitive
and intermediate hosts to complete their life cycle. There are 5 species of Schistosomes
responsible for human disease; S.
mansoni, S. haematobium and S.
japonicum with S. mekongi and S. intercalatum
being less common.
They are the only trematodes
that live in the blood stream of warm-blooded hosts. The blood stream is rich
in glucose, and amino acids, so along with the plasma and blood cells, it
represents an environment which is suitable for egg producing trematodes.
Over 200 million people are
infected over at least 75 countries with 500 million or more people exposed to
infection. With the disease spreading due to improved water supplies being
created therefore, forming potentially new habits for snails. The disease
caused is called schistosomiasis or
Bilharzia and is the most important of helminth diseases.
Infection by the three most
common species is the same in both sexes and in all age groups. Though, S.
mansoni and S. haematobium is seen to occur more often and most heavily in
teenagers especially males.
Adult worms of S. mansoni live in the plexus of veins draining the rectum and
colon, and in branches of the portal vein in the liver. (Fig. 12)
Diagram illustrating the general life cycle of the Schistosomes.
These trematodes are different from all of the others previously mentioned in
that they have separate sexes and inhabit the blood stream of warm-blooded
Adults of S. japonicum live in the anterior mesenteric blood vessels and in
the portal vein in the liver. Whilst the adults of S. haematobium live in the vesical plexus draining the bladder.
Once the eggs are laid by the
adult female worms the majority of them first pass through the veins of the
blood vessel in which the worm is living, and then into the lumen of the
intestine and are passed in the faeces (S.
mansoni and S. japonicum). Or
into the lumen of the bladder, and are then passed in the urine (S. haematobium). Those eggs that reach fresh water hatch, releasing
a miracidium which, to develop further must infect a snail of the correct
species within 24 hours. The eggs of each species are markedly different but
each produce virtually identical miracidium.
Asexual multiplication takes
place in the snail, and results in the release of cercariae (minute in size
with forked tails, 200mm long) into the water about 3
– 6 weeks later. Cercariae actively swim around and when they have located,
or come into contact with, a definitive host they actively penetrate the skin.
They can stay active looking for a host for 24 – 48 hours after which if
they don’t find a host they will die. The head of the cercariae migrates to
the liver and develops into either adult male or female worms (flukes), here
they pair up and then migrate to their region of the venous blood system
(species specific sites). The females leave the males and moves to smaller
venules closer to the lumen of the intestine or bladder to lay her eggs (about
6 weeks after infection). The majority of adult worms live from 2 – 4 years,
but some can live considerably longer.
in West and Central Africa, Egypt, Malagasy, the Arabian Peninsula, Brazil,
Surinam, Venezuela and the West Indies. The
intermediate host is an aquatic snail of the geuns Biomphalaria. Man is the most common definitive host, occasionally
baboons and rats are infected.
The adult worms live in
smaller branches of the inferior mesenteric vein in the lower colon.
The adult males measure up to 15 millimetres in
length and females up to 10 mm. The
schistosomes remain in copula throughout their life span, the uxorious male
surrounding the female with his gynaecophoric canal. (Fig.
13) The male is actually flat but the sides roll up forming the groove.
The cuticle of the male is covered with minute papillae. The female only
posses these at the anterior and posterior end as the middle section being
covered by the male body. Oral and ventral suckers are present, with the
ventral one being lager serving to hold the worms in place, preventing them
being carried away by the circulatory current.
Figure 13. Diagram
showing the coupling of the adult male and female S. mansoni worms as they would be in the inferior mesenteric veins
of the lower colon. The males hold the females within the gynaecophoric canal.
The ova of S. mansoni are 114-175mm long by 45-68mm
wide. They are light yellowish
brown, elongate and possess a lateral spine. (Fig.
14 & 15) The shell is acid fast when stained with modified
A non-viable egg is dark
coloured and shows no internal structural detail or flame cell movement.
Eggs can become calcified after treatment and are usually smaller,
appear black and often distorted with a less distinct spine.
15. Saline smear of a S. mansoni ova
showing clearly its lateral spine which is a good distinguishing factor when
identifying Schistosome ova. They
range in size between 114-175mm
long by 45-68mm
The schistosomes differ from other trematodes in
that they are dioecious, digenetic, their eggs are not operculate and
infection is acquired by penetration of cercaria through the skin.
The clinical disease is
related to the stage of infection, previous host exposure, worm burden and
host response. Cercarial
dermatitis (swimmers itch) follows skin penetration and results in a
maculopapular rash which may last 36 hours or more.
After mating, the mature
flukes migrate to the venules draining the large intestine.
Their eggs are laid and they penetrate the intestinal wall.
They are then excreted in
the faeces, often accompanied by blood and mucus.
It is the eggs and not the
adult worms, which are responsible for the pathology associated with S. mansoni infections. The
adult flukes acquire host antigen which protects them from the host's immune
The host's reaction to the
eggs which are lodged in the intestinal mucosa, leads to the formation of
granulomata and ulceration of the intestinal wall.
Some of the eggs reach the liver via the portal vein. The granulomatous
response to these eggs can result in the enlargement of the liver with
fibrosis, ultimately leading to portal hypertension and ascites. The spleen
may also become enlarged. Other
complications may arise as a result of deposition of the eggs in other organs
Katayama fever is associated
with heavy primary infection and egg production.
Clinical features include high fever, hepatosplenomegaly,
lymphadenopathy, eosinophilia and dysentery.
This syndrome occurs a few weeks after primary infection.
Laboratory confirmation of S.
mansoni infection can be made by finding the eggs in the faeces.
When eggs cannot be found in the faeces a rectal biopsy can be
tests are of value in the diagnosis of schistosomiasis when eggs cannot be
found. An enzyme linked
immunosorbent assay (ELISA) using soluble egg antigen, is employed at HTD.
japonicum is found in China, Japan, the
Philippines and Indonesia. It causes disease of the bowel with the eggs being
passed out in the faeces.
It differs form S.
mansoni and S. haematobium in
that it is a zoonosis in which a large number of mammals serve as reservoir
hosts, cats, dogs and cattle playing major roles in the transmission of the
The life cycle is not very different from that of S.
mansoni, the intermediate hosts are from the subspecies Oncomelania
hupensis. Sexual maturity is reach in about 4 weeks and eggs may be seen
in the faeces as quickly as 5 weeks.
They worms live coupled together in the superior,
mesenteric veins and desposit 1500 – 3500 eggs per day in the vessels of the
intestinal wall. The eggs infiltrate through the tissues and are passed in the
The adult worms are longer and narrower than the S.
mansoni worms. The ova are about 55 - 85mm by 40 - 60mm, oval with a minute lateral
spine or knob. (Fig 16)
The main lesions are again due to the eggs, occurring in the intestine
and liver. The eggs which are sequesters in the intestine mucosa or submucsa
initiate granulomatous reactions, resulting in the formation of
16. Saline smear of a S.
japonicum ova. They range in size between 55 - 85mm
by 40 - 60mm,
oval in shape with a minute lateral spine or knob. (Fig 14)
Due to the number of eggs released by the females the infection is more
severe than one with S. mansoni.
This is also due to the parasite being less well adapted to man, therefore,
the circumoval granuloma is very large. The intial illness can be prolonged
and sometimes fatal.
Laboratory confirmation of S.
japonicum infection can be made by finding the eggs in the faeces. When
eggs cannot be found in the faeces a rectal biopsy can be examined.
Other Schistosome species which are responsible for
human disease are S. mekongi and
S. intercalatum. These 2
species cause similar symptoms to that of S. mansoni and can be summarised in Table 3.
Mekong River basin
Central and west Africa
Stool, rectal biopsy,
Stool, rectal biopsy,
30-55 by 50-65mm
Oval, minute lateral spine
Elongate, terminal spine
Table 3. Table describing the
other less common intestinal Schistosome species that are known to cause disease in man.
different from the other two species previously mentioned in that it causes
urinary schistosomiasis. It occurs in Africa, India and the Middle East.
The intermediate host is the Bulinus
Just like S.
mansoni, its distribution runs parallel to the irrigation projects and in
areas which favour the intermediate hosts. They are exclusively parasites of
The mature worms live in copula mainly in the
inferior mesenteric veins and the females deposit their eggs in the walls of
the bladder and finally making their way into the urine. The life cycle is
very similar to that of S. mansoni,
with sexual maturity being reached within 4 – 5 weeks, but eggs may not
appear in the urine until 10 – 12 weeks or even later.
adult worms are longer than those of S.
mansoni. The ova are relatively large, measuring 110mm
in length and 40mm
in width. They have an elongated
ellipsoid shape with a prominent terminal spine. (Fig. 17)
haematobium eggs are elongated (110-170 by 40-70 microns) with
a prominent terminal spine. The
larva inside the egg produces an enzyme that passes through the egg-shell,
The clinical disease is related to the stage of
infection, previous host exposure, worm burden and host response.
Cercarial dermatitis (Swimmer’s Itch) following skin penetration,
results in a maculo-papular rash and can last 36 hours or more.
The mature flukes of S.
haematobium migrate to the veins surrounding the bladder.
After mating, the eggs are laid in the venules of the bladder and many
penetrate through the mucosa, enter the lumen of the bladder and are excreted
in the urine accompanied by blood. Thus
haematuria and proteinuria are characteristic, though not invariable features
of urinary schistosomiasis.
As with all
Schistosoma species, it is the eggs and not the adult worms which are
responsible for the pathology associated with S. haematobium. In
chronic disease, eggs become trapped in the bladder wall resulting in the
formation of granulomata. Following
prolonged infection, the ureters may become obstructed and the bladder becomes
thickened resulting in abnormal bladder function, urinary infection and kidney
damage. Chronic urinary
schistosomiasis is associated with squamous cell bladder cancer.
Heavy infections in males may involve the penis resulting in scrotal
lymphatics being blocked by the eggs.
The definitive diagnosis of urinary schistosomiasis
is made by finding the characteristic ova of S.
haematobium in urine. Terminal
urine should be collected as the terminal drops contain a large proportion of
the eggs. The urine can either be
centrifuged and the deposit examined microscopically for ova. Eggs can
sometimes be found in seminal fluid in males.
A bladder biopsy is seldom necessary to make the diagnosis.
A rectal snip may show the presence of ova as they sometimes pass into
the rectal mucosa.
Serological tests can be of value when eggs cannot
be found in clinical samples. An
enzyme linked immunosorbent assay using soluble egg antigen to detect
antischistosome antibody is most sensitive.
There is a marked periodicity associated with the time when most eggs are
passed out. Higher numbers of eggs are encountered in urine specimens passed
between 10 am and 2pm, presumably as a result of changes in the host’s
metabolic and physical activities.
Murray, PR, Drew, WL, Koyayashi, GS & Thomson,
JH: Medical Microbiology. Mosby Books
Inc., New York (1990)
Peters, W & Gilles, HM: Tropical Medicine & Parasitology. Wolfe Medical Publications
Jeffrey & Leach: Atlas
of Medical Helminthology and Protozoology. E & S Livingstone Ltd.
Ash, LR & Orihel, TC: Atlas of Human Parasitology. ASCP Press, Chicago.
Garcia, LS & Bruckner, DA: Diagnostic Medical Parasitology. Elsevior Science Publishing Co.
Muller, R & Baker, JR: Medical Parasitology. Gower Medical Publishing.
Snell, JJS, Farrell, ID & Roberts, C: Quality
Control, Principles and Practice in the Microbiology Laboratory. Public
Health Laboratory Service. ISBN 0 901 144 312.