AUTHOR AND EDITOR INFORMATION

Section 1 of 12  

• Authors and Editors
• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

INTRODUCTION

Section 2 of 12  

• Authors and Editors
• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Background

Numerous trematodes cause disease in humans. These include the schistosomes, which live in the gastrointestinal and genitourinary tracts, various liver flukes (eg, Clonorchis sinensis, Opisthorchiasis species), and the intestinal trematodes (flukes). This review focuses on only the intestinal trematodes.

Intestinal trematodes are flat hermaphroditic worms that vary in length from a few millimeters to many centimeters. Of the approximately 70 species known to colonize the human intestine, only a few species are known to cause actual infection.

The most common human intestinal trematode is Fasciolopsis buski. Infection involving the other 3 trematodes—Heterophyes heterophyes, Metagonimus yokogawai, and Echinostoma species—results in a presentation that is clinically similar to that of malabsorptive illness. In the genus Echinostoma, Echinostoma ilocanum is the most common organism that causes infection in humans. H heterophyes and M yokogawai are less-common causes of human intestinal fluke infection.

Other intestinal flukes that rarely cause human intestinal infection include Gastrodiscoides hominis, Phaneropsolus bonnei, and Prosthodendrium molenkampi.

Pathophysiology

Intestinal flukes cause inflammation, ulceration, and mucous secretion at the site of attachment. Severe infections may also cause intestinal obstruction or malabsorption, leading to hypoalbuminemia, protein-losing enteropathy, and impaired vitamin B-12 absorption.

F buski

F buski attaches to the duodenal and jejunal mucosa; however, in severe infections, it may attach to the ileum or colon.

In London, Busk first described F buski in 1843 after finding it in the duodenum of a sailor. In 1925, Barlow first determined its life cycle in humans (see Image 1). A well-known illustrative life cycle schematic (see Image 2) is shown below. The immature eggs (see Image 3) are discharged from human feces and reach fresh water, hatching after 3-7 weeks and forming miracidia. Upon contact with host snails, the miracidia penetrate the soft tissues and form sporocysts, first- and second-generation rediae, and, lastly, cercariae. The cercariae encyst on various plants such as water caltrop, water chestnut, lotus (on the roots), water bamboo, and other aquatic vegetables. Humans are infected by consuming these raw vegetables.

In the human duodenum, the metacercariae attach to the walls and become adult worms in approximately 3 months. The adult worm (see Image 4) causes traumatic, toxic, and obstructive damage to the intestinal mucosa. Deep inflammatory ulcerations develop at the site of attachment. Large numbers of worms provoke excess mucous discharge and can obstruct the lumen. The adult worm metabolites can also cause intoxication and sensitization when absorbed via the lumen.

Echinostoma species

In 1907, in Manila, Garrison first noted the genus Echinostoma, which is composed of 12 species reported to cause disease in humans. The most common species is E ilocanum, which has a characteristic horseshoe-shaped collar of 1-2 rows of straight spines that surround the dorsal and lateral sides of the oral sucker. E ilocanum are small, elongated flukes that measure 5-15 mm in length and 1-2 mm in width.

The adult worm, attached to the intestinal wall of humans, produces eggs that are passed in the feces. The eggs reach water, and miracidia develop and penetrate the first intermediate hosts—snails. During the course of 6-7 weeks inside the host snails, they develop into sporocysts, mother rediae, daughter rediae, and cercariae.

The cercariae leave the snails to encyst in the second intermediate hosts, which can be freshwater snails, fish, tadpoles, or vegetables. Humans are infected by ingesting raw or undercooked second intermediate hosts. Inside human hosts, the flukes then attach to the small intestinal mucosa and, depending on the severity of infection, can produce shallow ulcers with mild inflammation and/or local necrosis. Mild infections do not cause symptoms, but heavy infections produce diarrhea, flatulence, and intestinal colic similar to fasciolopsiasis.

H heterophyes

H heterophyes is the most common of the 10 species that compose the genus Heterophyes. H heterophyes is a small fluke, measuring 1-1.8 mm in length and 0.3-0.7 mm in width, with a broadly rounded posterior end. The oral sucker is subterminal and is one third the size of the ventral sucker.

H heterophyes are observed in the human intestine, jejunum, and ileum. The illustrative life cycle schematic for H heterophyes (see Image 5) is shown below. These worms produce eggs, which are excreted in the feces and into the water. The first intermediate hosts, the snails, ingest the eggs. In the snails, the eggs hatch and undergo their developmental cycle, forming cercariae, which emerge from the snails and encyst on the second intermediate hosts—brackish or freshwater fish. In the second intermediate hosts, the cercariae are transformed into metacercariae, which infect humans upon ingestion of raw or undercooked fish.

In humans, the flukes attach to the small bowel and cause shallow ulcers, mild inflammation, and/or superficial necrosis. Clinical presentation includes diarrhea, dyspepsia, and intestinal colic. Because of their small size, the eggs, and sometimes the adult flukes, enter blood vessels and embolize to the brain, producing symptoms similar to cerebral hemorrhage. Eggs may also enter the mesenteric lymphatics and travel to the heart, causing myocarditis, chronic congestive heart failure, and death.

M yokogawai

M yokogawai, which is closely related to H heterophyes, is another important parasite. M yokogawai measures 1-2.5 mm in length and 0.4-0.75 mm in width. The ventral sucker is located to the right of the midline.

M yokogawai has a life cycle similar to that of H heterophyes, in which the adult worm in the human intestine produces eggs that are excreted in the feces. The illustrative life cycle schematic for M yokogawai (see Image 6) is shown below. The eggs enter the water and infect the first intermediate hosts, the snails, where the eggs undergo their developmental cycle and become cercariae. Cercariae infect the second intermediate hosts, freshwater fish, and become metacercariae. Metacercariae infect humans after ingestion of raw or undercooked fish. The flukes then invade the mucosa of the small intestines, causing inflammation and ulcerations. Flukes eventually become encapsulated.

As in infection with H heterophyes, M yokogawai occasionally embolize to other organs. Patients infected with M yokogawai present with mucous, diarrhea, and vague abdominal symptoms. Prognosis is usually good, except in cases of embolization.

Frequency

United States

Infection with intestinal flukes affects only immigrants from endemic areas.

International

Intestinal flukes are endemic in the Far East and Southeast Asia. H Heterophyes can also be found in the Nile delta region of Egypt. The movement of migrant workers within and across various East Asian countries has led to an increase in the prevalence of intestinal flukes parasites (mainly F buski) into regions that were not previously endemic for intestinal flukes. 

Mortality/Morbidity

Death from infection is rare and usually occurs only in persons with a heavy worm burden who present with severe cachexia and prostration. Other intercurrent infection may also cause death. In cases of infection with H heterophyes or M yokogawai, death may occur after embolization of the eggs to the heart or brain. Embolization to the brain and spinal cord can also cause focal neurologic disease.

Race

Intestinal flukes are endemic in Asia and in some parts of North Africa, affecting groups who live in these areas.

Sex

Intestinal flukes have no predilection for either sex.

Age

Intestinal flukes can affect both children and adults, but children are affected more severely.

CLINICAL

Section 3 of 12  

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• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

History

Humans become infected with intestinal flukes by consuming contaminated food and water that consists of or contains the second intermediate hosts (eg, vegetation, snails, fish).

• Most infected persons are asymptomatic and exhibit no physical signs.
• Individuals with moderate infection present with occasional loose stools, some weight loss, malaise, and, occasionally, generalized abdominal pain.
• Severe infection, in which toxic diarrhea alternating with constipation and hunger pangs are the first symptoms to appear, usually occurs near the end of the incubation period. As the infection progresses and the worm burden increases, edema of the face, abdominal wall, and lower limbs occurs, as well as ascites and generalized abdominal pain. Anorexia, nausea, and vomiting are also common. The diarrhea persists, becoming greenish-yellow and exceptionally malodorous.
• In persons infected with H heterophyes, embolization of the eggs can lead to myocarditis, chronic heart failure, and/or cerebral emboli.

Physical

• In mild infections, patients are asymptomatic on physical examination.
• In severe infections, patients are asthenic, with gray and harsh skin and edema of the face and lower extremities.

Causes

Intestinal flukes are endemic in areas that contain abundant snail hosts (eg, China, Vietnam, India, other parts of Asia. 

Table 1. Common Intestinal Trematode Infections*

*Adapted with permission from Tribble D, Wagner KF. Trematode infections. Infectious Disease Practice. 1996;20:69-73.

Table 2. Commonly Associated Exposures and Clinical Features of Certain Intestinal Trematodes*

DIFFERENTIALS

Section 4 of 12  

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• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Other Problems to be Considered

Differential diagnoses of trematode eggs in feces include other trematodes, such as liver flukes or lung flukes (see below¹ and see Table 1).

• Intestinal flukes
• • Frequently asymptomatic
  • Mild infection - Mild diarrhea, abdominal pain
  • Severe infection - Malabsorption, intestinal obstruction, eosinophilia may be present
• Liver flukes (opisthorchiasis, clonorchiasis)
• • Frequently asymptomatic
  • Acute infection - Serum sickness–like illness (similar to Katayama fever with high fever, eosinophilia, tender hepatomegaly, rash)
  • Advanced stage - May be complicated by recurrent cholangitis, jaundice, associated with cholangiocarcinoma
• Liver flukes (fascioliasis)
• • Acute infection - High fever, right-upper-quadrant pain, hepatomegaly, eosinophilia, urticaria
  • Chronic stage - Frequently asymptomatic, biliary obstructive symptoms, eosinophilia
  • Ectopic infection - Visceral larva migrans–like, aberrant sites (eg, lungs, heart, brain, skin)
• Lung flukes (paragonimiasis)
• • Acute infection - Diarrhea and pain, eosinophilia, fever, cough, dyspnea, chest pain
  • Pulmonary stage (after approximately 6 mo) - Chronic bronchitis symptoms progressing to pleurisy, hemoptysis, eosinophilia, pulmonary infiltrates with cysts, with or without thin-walled cavities and pleural effusions
  • Cerebrospinal infection - Brain or spinal cord invasion with 1-10 cysts, meningoencephalitis or paraplegia in symptomatic infections (acute infections)
  • Abdominal infection - Invasion into liver, spleen, or peritoneum
  • Migratory subcutaneous infection - Firm, slightly mobile, tender cysts similar to trematode larva migrans

WORKUP

Section 5 of 12  

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• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Lab Studies

• Stool examination to visualize the ova or adult worms is the diagnostic method of choice.
• Other laboratory findings include anemia and eosinophilia.
• No serologic tests are available.

Other Tests

• Merthiolate, iodine, formalin method
• • The merthiolate, iodine, formalin (MIF) method is used to detect intestinal fluke parasites.
  • The MIF method was established early as a versatile and accurate technique for identifying intestinal protozoa in stool and fecal samples.² The technique simultaneously preserves and stains stool specimens, which can then be examined with direct smear techniques.³
  • Following the development of a concentrated MIF technique, the sensitivity of positively identifying F buski, Heterophyes species, and Echinostoma species in stool specimens was increased.⁴ This newly concentrated MIF technique involves the application of a concentration step to the stool specimen before preservation in MIF solution.
• Polymerase chain reaction
• • Various polymerase chain reaction (PCR) methods have shown potential in detecting intestinal fluke parasites. These methods take advantage of the different types of DNA nucleotide sequence variations demonstrated by the different species of parasites within a particular genus. 
  • Polymerase chain reaction–restriction fragment length polymorphism (PCR-RFLP)⁵ and simple sequence repeat anchored PCR⁶ have been reported to be useful in distinguishing among species of the Metagonimus genus (including M yokogawai). These methodologies are based on differences in restriction fragment length polymorphisms and simple sequence repeats among the species. 
  • Six species of the genus Heterophyidae were reported to be distinguished with PCR assays developed based on variations in rDNA polymorphisms among the species.⁷

TREATMENT

Section 6 of 12  

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• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Medical Care

Symptoms and infection may resolve without therapy, although treatment can be provided with praziquantel (20 mg/kg PO q8h for 1 d).
 
Praziquantel is recommended when bithionol (used primarily for Fasciola infection) is not available. In some cases, intercurrent bacterial infections occur that may then be treated with the appropriate antibiotic therapy (in the inpatient or outpatient setting).

Diet

• Proper cleaning and processing of raw vegetables by immersing in boiling water for a few seconds, followed by peeling and washing in clean water is important in preventing infection with intestinal flukes, especially in endemic areas.
• The importance of thoroughly cooking contaminated vegetables cannot be overemphasized.
• Do not eat raw or undercooked fish.
• The diet in infected individuals should contain adequate protein.

Activity

The patient should be on bed rest.

MEDICATION

Section 7 of 12  

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The goals of pharmacotherapy are to reduce morbidity, to prevent complications, and to eradicate the infection.

Drug Category: Anthelmintics

The biochemical pathways in parasites are different enough from those of the human host to allow selective interference with chemotherapeutic agents in relatively small doses.

FOLLOW-UP

Section 8 of 12  

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• Introduction
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• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Further Inpatient Care

• Antispasmodics may relieve abdominal pain.
• Iron supplements may be used to treat anemia, which may require transfusions in severe cases.
• Vitamin C (ascorbic acid) may be administered to facilitate iron absorption.

Further Outpatient Care

• Health education is essential; proper washing and thorough cooking of vegetables or fish are essential to prevent egg ingestion.

Deterrence/Prevention

• Eliminating the intermediate host snail is the key to controlling infection with intestinal flukes.
• Proper cleaning and processing of raw vegetables by immersing in boiling water for a few seconds, followed by peeling and washing in clean water, is important in preventing infection with intestinal flukes, especially in endemic areas.
• Night soil (human excreta) and pig excreta should not be used as fertilizers.
• Metacercariae are not necessarily inhibited or destroyed by interventions such as smoking or freezing; and the practice of fish pickling is ineffective. Irradiation practices may be of benefit in managing the burden of metacercariae in the process of food preparation.

Prognosis

• Light infections may resolve spontaneously within one year, even without treatment. The prognosis may be grave in patients with heavy infection.

Patient Education

• Instruct patients on proper food preparation to avoid infection with intestinal flukes. Thoroughly cooking fish and mollusks is always recommended.
• Educational interventions that emphasize avoidance of fecal contamination of water where fish and aquatic plants thrive are recommended to prevent intestinal trematode infections.

MISCELLANEOUS

Section 9 of 12  

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• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Medical/Legal Pitfalls

Failure to diagnose is possible; thus, a clear and thorough exposure history must be obtained. Additionally, the differential diagnoses may be broad; accordingly, consider other etiologies of symptoms such as nausea, vomiting, abdominal cramps, fever, and diarrhea, as well other mild symptoms. Based on best practices, treatment is most successful when patients carefully follow the prescribed treatment, promptly report any side effects and toxicities, and report any lack of adherence.

ACKNOWLEDGMENTS

Section 10 of 12  

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• Miscellaneous
• Acknowledgments
• Multimedia
• References

The author would like to acknowledge Paul Chen, BS, ScM (2008) in Genetic Epidemiology, Johns Hopkins University Bloomberg School of Public Health, whose contributions and insights were invaluable for the revision of this article.

MULTIMEDIA

Section 11 of 12  

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• Clinical
• Differentials
• Workup
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• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

Media file 1:  Life cycle of Fasciolopsis buski. Image reproduced from the Division of Parasitic Disease, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media file 2:  The life cycle of Fasciolopsis. Immature eggs are discharged into the intestine and stool and become embryonated in water. The eggs then release miracidia, which invade a suitable snail intermediate host, in which the parasites undergo several developmental stages (sporocysts, rediae, cercariae). The cercariae are released from the snail and encyst as metacercariae on aquatic plants, which are eaten by mammalian hosts (humans and pigs), who become infected. After ingestion, the metacercariae excyst in the duodenum and attach to the intestinal wall, where they develop into adult flukes (20-75 mm X 8-20 mm) in approximately 3 months and attach to the intestinal wall of the mammalian hosts. The adults have a life span of about one year. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media type:  Illustration

Media file 3:  Egg of Fasciolopsis buski. Images reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media type:  Photo

Media file 4:  Adult fluke of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media type:  Photo

Media file 5:  The life cycle of Heterophyes. The adult parasites release embryonated eggs (each with a fully developed miracidium), which are then passed in the host's feces. After ingestion by a suitable snail (first intermediate host), the eggs hatch and release miracidia, which penetrate the snail's intestine. Snails of the genera Cerithidea and Pirenella are important hosts in Asia and the Middle East, respectively. The miracidia undergo several developmental stages in the snail (sporocysts, rediae, cercariae). Many cercariae are produced from each redia. The cercariae are released from the snail and encyst as metacercariae in the tissues of a suitable freshwater or brackish-water fish (second intermediate host). The definitive host becomes infected by ingesting undercooked or salted fish that contains metacercariae. After ingestion, the metacercariae excyst, attach to the mucosa of the small intestine, and mature into adults (measuring 1-1.7 mm X 0.3-0.4 mm). Heterophyes heterophyes infects humans, various fish-eating mammals (eg, cats, dogs), and birds. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media type:  Illustration

Media file 6:  Life cycle of Metagonimus. The adult parasites release fully embryonated eggs (each with a fully developed miracidium), which are then passed in the host's feces. After ingestion by a suitable snail (first intermediate host), the eggs hatch and release miracidia, which penetrate the snail's intestine. Snails of the genus Semisulcospira are the most common intermediate host for Metagonimus yokogawai. The miracidia undergo several developmental stages in the snail (sporocysts, rediae, cercariae). Many cercariae are produced from each redia. The cercariae are released from the snail and encyst as metacercariae in the tissues of a suitable freshwater or brackish-water fish (second intermediate host). The definitive host becomes infected by ingesting undercooked or salted fish that contains metacercariae. After ingestion, the metacercariae excyst, attach to the mucosa of the small intestine, and mature into adults (measuring 1-2.5 mm X 0.4-0.75 mm). M yokogawai infects humans, fish-eating mammals (eg, cats, dogs), and birds. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Ga.
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Media type:  Illustration

REFERENCES

Section 12 of 12

• Authors and Editors
• Introduction
• Clinical
• Differentials
• Workup
• Treatment
• Medication
• Follow-up
• Miscellaneous
• Acknowledgments
• Multimedia
• References

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Article Last Updated: Dec 14, 2007