eMedicine Specialties > Infectious Diseases > Parasitic Infections
Intestinal Flukes
Updated: Dec 14, 2007
Introduction
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
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*
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Table
| Infection | Source | Geographic Distribution |
|---|---|---|
| Fasciolopsiasis | Freshwater plants (water caltrop, water chestnut) | China, Thailand, Bangladesh, India |
| Echinostomiasis | Tadpoles, freshwater snails, fish, frogs | Indonesia, Philippines, Taiwan, Thailand |
| Heterophyiasis | Fish | Egypt, Iran, Tunisia, Turkey |
| Metagonimiasis | Fish (cyprinid) | Far East, Spain, Eastern Europe |
| Infection | Source | Geographic Distribution |
|---|---|---|
| Fasciolopsiasis | Freshwater plants (water caltrop, water chestnut) | China, Thailand, Bangladesh, India |
| Echinostomiasis | Tadpoles, freshwater snails, fish, frogs | Indonesia, Philippines, Taiwan, Thailand |
| Heterophyiasis | Fish | Egypt, Iran, Tunisia, Turkey |
| Metagonimiasis | Fish (cyprinid) | Far East, Spain, Eastern Europe |
*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*
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Table
| Infection | Source | Clinical Features |
|---|---|---|
| Alaria americana | Undercooked frog legs | Disseminated fatal thoracic, gastrointestinal, retroperitoneal, and CNS manifestations; intraocular infections |
| Echinostomiasis (16 species) | Freshwater fish, aquatic plants, clams, snails, mollusks, contact with aquatic birds | May be asymptomatic; mild abdominal pain, bloating, dyspepsia, diarrhea, eosinophilia |
| Fibricola species | Tadpoles | Abdominal pain, diarrhea, fever, eosinophilia |
| Fasciolopsis species | Water chestnut, water calthrop, water bamboo, water morning glory lotus and water hyacinth | May be symptomatic; may be subclinical; gastritis, nausea, diarrhea, eosinophilia; generalized edema in persons with heavy infection burden |
| Gastrodiscoides species | Vegetables, aquatic plants | Often asymptomatic; may manifest as abdominal pain and diarrhea in severe cases |
| Watsonius watsoni | Water bamboo | Severe diarrhea |
| Fischoederius elongates | Aquatic plants | Epigastric pain and vomiting |
| Heterophyes species | Mullets, fish; brackish water | May be asymptomatic; intestinal mucosal disease, ulcer-related abdominal pain, dyspepsia, nausea, vomiting, diarrhea, weight loss |
| Gymnophalloides seoi | Oysters | Fever, abdominal pain, anorexia, weight loss, diarrhea, pancreatitis |
| Carneophallus brevicaeca | Shrimp | Fatal when infection involves CNS and heart |
| Brachylaima ruminae | Poultry, rats | Abdominal pain, diarrhea |
| Metagonimiasis species | Fish (ayu, golden carp) | May be asymptomatic; intestinal mucosal disease, ulcer-related abdominal pain, dyspepsia, nausea, vomiting, diarrhea, weight loss |
| Nanophyetus salmincola | Undercooked fish (eg, salmon, trout, steelhead) | May be symptomatic; mild diarrhea, abdominal pain |
| Infection | Source | Clinical Features |
|---|---|---|
| Alaria americana | Undercooked frog legs | Disseminated fatal thoracic, gastrointestinal, retroperitoneal, and CNS manifestations; intraocular infections |
| Echinostomiasis (16 species) | Freshwater fish, aquatic plants, clams, snails, mollusks, contact with aquatic birds | May be asymptomatic; mild abdominal pain, bloating, dyspepsia, diarrhea, eosinophilia |
| Fibricola species | Tadpoles | Abdominal pain, diarrhea, fever, eosinophilia |
| Fasciolopsis species | Water chestnut, water calthrop, water bamboo, water morning glory lotus and water hyacinth | May be symptomatic; may be subclinical; gastritis, nausea, diarrhea, eosinophilia; generalized edema in persons with heavy infection burden |
| Gastrodiscoides species | Vegetables, aquatic plants | Often asymptomatic; may manifest as abdominal pain and diarrhea in severe cases |
| Watsonius watsoni | Water bamboo | Severe diarrhea |
| Fischoederius elongates | Aquatic plants | Epigastric pain and vomiting |
| Heterophyes species | Mullets, fish; brackish water | May be asymptomatic; intestinal mucosal disease, ulcer-related abdominal pain, dyspepsia, nausea, vomiting, diarrhea, weight loss |
| Gymnophalloides seoi | Oysters | Fever, abdominal pain, anorexia, weight loss, diarrhea, pancreatitis |
| Carneophallus brevicaeca | Shrimp | Fatal when infection involves CNS and heart |
| Brachylaima ruminae | Poultry, rats | Abdominal pain, diarrhea |
| Metagonimiasis species | Fish (ayu, golden carp) | May be asymptomatic; intestinal mucosal disease, ulcer-related abdominal pain, dyspepsia, nausea, vomiting, diarrhea, weight loss |
| Nanophyetus salmincola | Undercooked fish (eg, salmon, trout, steelhead) | May be symptomatic; mild diarrhea, abdominal pain |
*Adapted from Berger SA, Marr JS. Human Parasitic Diseases Sourcebook. 1st ed. Sudbury, MA: Jones and Bartlett; 2006.
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References
Tribble D, Wagner KF. Trematode infections. Infectious Disease Practice. 1996;20:69-73.
Sapero JJ, Lawless DK. The MIF stain-preservation technic for the identification of intestinal protozoa. Am J Trop Med Hyg. Jul 1953;2(4):613-9. [Medline]. [Full Text].
Price DL. Comparison of three collection-preservation methods for detection of intestinal parasites. J Clin Microbiol. Dec 1981;14(6):656-60. [Medline]. [Full Text].
Wang LC. Improvement in the identification of intestinal parasites by a concentrated merthiolate-iodine-formaldehyde technique. J Parasitol. April 1998;84(2):457-8. [Medline].
Yu JR, Chung JS, Huh S, Lee SH, Chai JY. PCR-RFLP pattern of three kinds of Metagonimus in Korea. Korean J Parasitol. Dec 1997;35(4):271-6. [Medline].
Yang HJ, Guk SM, Han ET, Chai JY. Molecular differentiation of three species of Metagonimus by simple sequence repeat anchored polymerase chain reaction (SSR-PCR) amplification. J Parasitol. Oct 2000;86(5):1170-2. [Medline].
Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I. Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis Aquat Organ. Apr 21 2004;59(1):35-41. [Medline].
Adams M, Motarjemi Y. Basic Food Safety for Health Workers. Geneva: World Health Organization; 1999.
Ahn YK. [Intestinal flukes of genus Metagonimus and their second intermediate hosts in Kangwon-do]. Korean J Parasitol. Dec 1993;31(4):331-40. [Medline].
Belizario, VY Jr, Bersabe, MJ, de Leon, WU, et al. Intestinal heterophyidiasis: an emerging food-borne parasitic zoonosis in southern Philippines. Southeast Asian J Trop Med Public Health. 2001;32; Suppl 2:36-42. [Medline].
Berger SA, Marr JS. Human Parasitic Diseases Sourcebook. First ed. Sudbury, MA: Jones and Bartlett; 2006.
Bunnag D, Radomyos P, Harinasuta T. Field trial on the treatment of fasciolopsiasis with praziquantel. Southeast Asian J Trop Med Public Health. Jun 1983;14(2):216-9. [Medline].
Bunnag T, Sornmani S, Impand P. Potential health hazards of the water resources development: a health survey in the Phitsanulok Irrigation Project, Nan River Basin, Northern Thailand. Southeast Asian J Trop Med Public Health. Dec 1980;11(4):559-65. [Medline].
Chai JY, Kim IM, Seo M. A new endemic focus of Heterophyes nocens, Pygidiopsis summa, and other intestinal flukes in a coastal area of Muan-gun, Chollanam-do. Korean J Parasitol. Dec 1997;35(4):233-8. [Medline].
Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int. Jun 2002;51(2):129-54. [Medline].
Chandra SS. Epidemiology of Fasciolopsis buski in Uttar Pradesh. Indian J Med Res. Jan 1984;79:55-9. [Medline].
Chung DI, Moon CH, Kong HH, Choi DW, Lim DK. The first human case of Clinostomum complanatum (Trematoda: Clinostomidae) infection in Korea. Korean J Parasitol. Sep 1995;33(3):219-23. [Medline].
Drugs For Parasitic Infections. The Medical Letter. August 2004;46(1189):e1-e12.
Drugs for Parasitic Infections. Medical Let Drugs Ther. 2004;[Full Text].
Eastburn RL, Fritsche TR, Terhune CA Jr. Human intestinal infection with Nanophyetus salmincola from salmonid fishes. Am J Trop Med Hyg. May 1987;36(3):586-91. [Medline].
Eckert J. Workshop summary: food safety: meat- and fish-borne zoonoses. Vet Parasitol. Aug 1996;64(1-2):143-7. [Medline].
Fernandes BJ, Cooper JD, Cullen JB, Freeman RS, Ritchie AC, Scott AA. Systemic infection with Alaria americana (Trematoda). Can Med Assoc J. Dec 4 1976;115(11):1111-4. [Medline].
Gai L, Ma X, Fu Y, Huang D. [Relationship between the rate of parasitic infection and the knowledge of prevention]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 1995;13(4):269-72. [Medline].
Gajadhar AA, Scandrett WB, Forbes LB. Overview of food- and water-borne zoonotic parasites at the farm level. Rev Sci Tech. Aug 2006;25(2):595-606. [Medline].
Gilman RH, Mondal G, Maksud M. Endemic focus of Fasciolopsis buski infection in Bangladesh. Am J Trop Med Hyg. Jul 1982;31(4):796-802. [Medline].
Graczyk TK, Fried B. Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg. Apr 1998;58(4):501-4. [Medline].
Graczyk TK, Gilman RH, Fried B. Fasciolopsiasis: is it a controllable food-borne disease?. Parasitol Res. Jan 2001;87(1):80-3. [Medline].
Hadidjaja P, Dahri HM, Roesin R. First autochthonous case of Fasciolopsis buski infection in Indonesia. Am J Trop Med Hyg. Sep 1982;31(5):1065. [Medline].
Harinasuta T, Bunnag D, Radomyos P. Efficacy of praziquantel on fasciolopsiasis. Arzneimittelforschung. 1984;34(9B):1214-5. [Medline].
Kaul BK, Singhal GD, Pillai PN. Artyfechinostomum mehrai infestation with bowel perforation. J Indian Med Assoc. Oct 16 1974;63(8):263-5. [Medline].
Kumar V. The digenetic trematodes, Fasciolopsis buski, Gastrodiscoides hominis and Artyfechinostomum malayanum, as zoonotic infections in South Asian countries. Ann Soc Belg Med Trop. Dec 1980;60(4):331-9. [Medline].
Liu LX, Harinasuta KT. Liver and intestinal flukes. Gastroenterol Clin North Am. Sep 1996;25(3):627-36. [Medline].
Lo CT, Lee KM. Intestinal parasites among the Southeast Asian laborers in Taiwan during 1993-1994. Zhonghua Yi Xue Za Zhi (Taipei). Jun 1996;57(6):401-4. [Medline].
Maclean JD, Cross J, Mahanty S. Liver, lung, and intestinal fluke infections. In: Guerrant RL, Walker DH, Weller PF, eds. Tropical Infectious Diseases: Principles, Pathogens and Practice. 2nd ed. Philadelphia, PA: Churchill Livingstone; 2006:1349 ff.
Malviya HC. The susceptibility of mammals to Fasciolopsis buski. J Helminthol. Mar 1985;59(1):19-22. [Medline].
Manjarumkar PV, Shah PM. Epidemiological study of Fasciolopsis Buski in Palghar Taluk. Indian J Public Health. Jan 1972;16(1):3-6. [Medline].
Manning GS, Ratanarat C. Fasciolopsis buski (Lankester, 1857) in Thailand. Am J Trop Med Hyg. Jul 1970;19(4):613-9. [Medline].
McDonald HR, Kazacos KR, Schatz H, Johnson RN. Two cases of intraocular infection with Alaria mesocercaria (Trematoda). Am J Ophthalmol. Apr 15 1994;117(4):447-55. [Medline].
Muttalib MA, Islam N. Fasciolopsis buski in Bangladesh-a pilot study. J Trop Med Hyg. Jun 1975;78(6):135-7. [Medline].
Park JH, Kim JL, Shin EH, Guk SM, Park YK, Chai JY. A new endemic focus of Heterophyes nocens and other heterophyid infections in a coastal area of Gangjin-gun, Jeollanam-do. Korean J Parasitol. Mar 2007;45(1):33-8. [Medline]. [Full Text].
Plaut AG, Kampanart-Sanyakorn C, Manning GS. A clinical study of Fasciolopsis buski infection in Thailand. Trans R Soc Trop Med Hyg. 1969;63(4):470-8. [Medline].
Pungpak S, Radomyos P, Radomyos BE. Treatment of Opisthorchis viverrini and intestinal fluke infections with Praziquantel. Southeast Asian J Trop Med Public Health. Jun 1998;29(2):246-9. [Medline].
Radomyos B, Wongsaroj T, Wilairatana P. Opisthorchiasis and intestinal fluke infections in northern Thailand. Southeast Asian J Trop Med Public Health. Mar 1998;29(1):123-7. [Medline].
Radomyos P, Radomyos B, Tungtrongchitr A. Multi-infection with helminths in adults from northeast Thailand as determined by post-treatment fecal examination of adult worms. Trop Med Parasitol. Jun 1994;45(2):133-5. [Medline].
Shah PM, Udani PM, Manjarumkar PV. Fasciolopsis Buski infestation in children. Indian Pediatr. Dec 1973;10(12):721-4. [Medline].
Suntharasamai P, Bunnag D, Tejavanij S. Comparative clinical trials of niclosamide and tetrachlorethylene in the treatment of Fasciolopsis buski infection. Southeast Asian J Trop Med Public Health. Dec 1974;5(4):556-9. [Medline].
Taraschewski H, Mehlhorn H, Bunnag D. Effects of praziquantel on human intestinal flukes (Fasciolopsis buski and Heterophyes heterophyes). Zentralbl Bakteriol Mikrobiol Hyg [A]. Nov 1986;262(4):542-50. [Medline].
Waikagul J. Intestinal fluke infections in Southeast Asia. Southeast Asian J Trop Med Public Health. Dec 1991;22 Suppl:158-62. [Medline].
Wegner DH. The profile of the trematodicidal compound praziquantel. Arzneimittelforschung. 1984;34(9B):1132-6. [Medline].
Wiwanitkit V, Nithiuthai S, Suwansaksri J. Motility of minute intestinal fluke, Haplorchinae spp, metacercariae in fish dishes prepared by different uncooked methods. MedGenMed. Mar 6 2002;4(1):8. [Medline].
Wiwanitkit V, Suwansaksri J, Chaiyakhun Y. High prevalence of Fasciolopsis buski in an endemic area of liver fluke infection in Thailand. MedGenMed. Jul 9 2002;4(3):6. [Medline].
Xu L, Jiang Z, Yu S. [Characteristics and recent trends in endemicity of human parasitic diseases in China]. Chung Kuo Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih. 1995;13(3):214-7. [Medline].
Further Reading
Keywords
intestinal flukes, intestinal trematodes, intestinal parasites, fasciolopsiasis, Fasciolopsis buski, F buski, Echinostoma ilocanum, E ilocanum, Heterophyes heterophyes, H heterophyes, Metagonimus yokogawai, M yokogawai, Gastrodiscoides hominis, G hominis, Phaneropsolus bonnei, P bonnei, Prosthodendrium molenkampi, P molenkampi,, fasciolopsiasis, echinostomiasis, heterophyiasis, heterophyidiasis, metagonimiasis, fluke infection
Overview: Intestinal Flukes