Sections

Sections Intestinal Flukes
Overview
Presentation
- History
- Physical
- Causes
- Show All
DDx
Workup
Treatment
Medication
Media Gallery
Tables
References

Overview

Background

Numerous trematodes cause disease in humans. Flukes that cause schistosomiasis, paragonimiasis, fascioliasis, clonorchiasis, and opisthorchiasis are included in the World Health Organization (WHO) list of neglected tropical diseases (NTD) to which interventions for poor and marginalized populations are prioritized given the significant health burden.^{[1, 2, 3]}Although this article focuses on intestinal trematodes, a limited discussion on liver flukes (Clonorchis sinensis, Opisthorchis viverrini, Fasciola hepatica, Fasciola gigantica) is provided given the similarity in the mode of acquisition (foodborne) and the challenge in terms of diagnostic differentiation with the intestinal flukes.

Intestinal trematodes can be classified into at least 14 families (with their corresponding sources of infection found below), as follows^[4]:

Brachylaimidae (from terrestrial snails)
Cathaemasiidae (from a yet unknown source)
Diplostomidae (from snakes, frogs, and tadpoles)
Echinostomatidae (from freshwater fish, frogs, mussels, snails, and tadpoles)
Fasciolidae (from aquatic vegetables and contaminated water)
Gastrodiscidae (from aquatic vegetables, crustaceans, molluscs, and amphibians)
Gymnophallidae (from oysters)
Heterophyidae (freshwater fishes)
Lecithodendriidae (from dragonflies)
Microphallidae (from shrimps and crabs)
Nanophyetidae (from salmonid fishes)
Paramphistomidae (from aquatic plants)
Plagiorchiidae (from insect larvae)
Strigeidae (from a yet unknown source)

Intestinal trematodes are flat hermaphroditic worms that vary in length from a few millimeters to many centimeters (see the image below). Of the approximately 70 species known to colonize the human intestine, only a few species are known to cause actual infection. Globally, it is likely that more than the estimated 40-50 million people are infected with intestinal trematodes, primarily infected via the foodborne route. Populations in Southeast Asia appear to be most vulnerable. An exhaustive 2009 review of these infections in this region provides detailed information on the large number of species infecting humans, their pathogenicity, diagnostic issues, and treatments.^[5]

In 2012, the various manifestations, methods of diagnosis, and management of foodborne trematodiasis, which include the intestinal flukes, were detailed in the British Medical Journal^[6]and the European Journal of Microbiology and Infectious Diseases.^[7] In the former, the species of intestinal flukes considered to be of public importance include the following:

Echinostoma species
Fasciolopsis buski
Gymnophalloides seoi
Haplorchis species
Heterophyes species
Metagonimus species

Adult fluke of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.

View Media Gallery

The most common human intestinal trematode was said to be Fasciolopsis buski, which causes fasciolopsiasis,^[8]and should be differentiated from Fasciola hepatica and Fasciola gigantica, which are liver flukes that cause fascioliasis. Conversely, the genus Echinostoma is the largest, with about 500 species of echinostomatid flukes. About 20 species belonging to 10 genera have been reported to cause human disease.^[9]The genus Echinostoma is considered the largest, which includes Echinostomahortense, Echinostomaangustitestis, Echinostomacinetorchis, Echinostomaechinatum, Echinostoma ilocanum, Echinostomamacrorchis, and Echinostomarevolutum. E ilocanum was said to be the most common cause of infection in humans.^{[1, 10]}

Heterophyes heterophyes, Metagonimus yokogawai, and Gymnophalloides species are less-common causes of human intestinal fluke infection.^[1]

Other intestinal flukes that rarely cause human intestinal infection include Gastrodiscoides hominis, Phaneropsolus bonnei, and Prosthodendrium molenkampi. Intestinal flukes have likely infected humans for hundreds of years, if not longer. Evidence of G seoi infection has been traced back to the 17th century based on discovery of G seoi eggs in a Korean mummy.^{[1, 11]}

See Common Intestinal Parasites, a Critical Images slideshow, to help make an accurate diagnosis.

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. Foodborne illness has been associated with the ingestion of many different types of potentially infected foods, such as different types of both freshwater and brackish-water fish and snails, reptiles (amphibians and certain snakes), aquatic plants, and insects.^[5]

Fasciolopsis buski

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

In London, Busk first described Fasciolopsis buski in 1843 after finding it in the duodenum of a sailor. In 1925, Barlow first determined its life cycle in humans. A well-known illustrative life cycle schematic is shown below.

Life cycle of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.

View Media Gallery

The immature eggs (see the images below) are discharged from human feces and reach fresh water, hatching after 3-7 weeks and forming miracidia.

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.

View Media Gallery

Egg of Fasciolopsis buski. Images reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.

View Media Gallery

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 below) 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. A recent case report provides evidence of heavy infestation as a risk factor for intestinal perforation.^[12]

Adult fluke of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.

View Media Gallery

Echinostoma species

In 1907, in Manila, Garrison first noted the genus Echinostoma, which is reported to have 12 species that may 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 flukes are small and elongated, measuring 5-15 mm in length and 1-2 mm in width. The most well-studied human-infecting species is E hortense.^[13]

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. Although not directly applicable to the human host, data in rodents suggest that, depending on trematode species, host species, and strain, primary expulsion of the fluke may occur.^{[14, 15]}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.

Disease manifestations in humans likely result from two pathogenetic mechanisms, including fluke-induced mechanical irritation and/or the related allergic reaction to various toxic metabolites.^[13]Humoral responses to echinostomal infections may include elevated serum and gut-associated immunoglobulin A (IgA), immunoglobulin G (IgG), and immunoglobulin M (IgM) levels, as demonstrated by studies involving Echinostoma caproni.^[16]

The intestinal epithelium appears to provide an important mechanism in mucosal defense. Its rapid epithelial cell turnover seems to facilitate the rejection of intestinal helminths. In rats, it has been shown that E caproni infection stimulates the augmented renewal of the intestinal epithelium, preventing the parasite from establishing itself in the host, resulting in clearance of the helminth.^[17]

Various animals may be definitive hosts for different Echinostoma species, such as aquatic birds, carnivores, rodents, and humans. Unembryonated eggs are passed in stool (1), and development occurs in the water (2). The miracidium takes an average of 10 days to mature and then hatches (3), penetrating the first intermediate host, a snail (4). Snails, in general, serve as the first intermediate host. The intramolluscan stages are as follows: sporocyst (4a); rediae (4b); and cercariae (4c). Cercariae may then encyst as metacercariae in the same first intermediate host or leave to penetrate a new second intermediate host (5). Several animals may become the second intermediate host, such as other snails, bivalves, fish, and tadpoles. The definitive host gets infected after eating infected second intermediate hosts (6). The metacercariae excyst in the duodenum (7). Adults then live in the small intestine (8). Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.

View Media Gallery

Heterophyes 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 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. See the image below.

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.

View Media Gallery

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.

Metagonimus 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 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.

See the image below.

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.

View Media Gallery

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. Fortunately, health studies performed in 2006 indicate that M yokogawai species and infections have become less endemic in certain regions.^[18]

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. Table 1 shows the geographic distribution and source of most commonly reported intestinal trematodes. The list of countries where human trematode infections have been reported is long, with several studies indicating variable incidence rates.^{[19, 20, 21, 5, 22, 23, 24, 10, 25, 26, 27]}

Table 1. Common Intestinal Trematode Infections (Open Table in a new window)

Infection	Source*	Geographic Distribution**
Fasciolopsiasis	Freshwater plants (water caltrop, water chestnut)	Asia and Indian subcontinent, especially in areas where humans raise pigs and consume freshwater plants (as of December 8, 2017)
Echinostomiasis	Tadpoles, freshwater snails, fish, frogs	Worldwide, but human cases seen most frequently in Southeast Asia and in areas where undercooked or raw freshwater snails, clams, and fish are eaten (as of December 27, 2017)
Heterophyiasis	Fish	Egypt, Middle East, Far East (as of January 3, 2018)
Metagonimiasis	Fish (cyprinid)	Far East, Siberia, Manchuria, the Balkan states, Israel, Spain (as of December 29, 2017)
* Adapted with permission from Tribble D, Wagner KF. Trematode infections. Infectious Disease Practice. 1996; 20:69-73. ** Updated data from the Centers for Disease Control and Prevention (DPDx Laboratory Identification of Parasites of Public Health Concern. Available: http://www.cdc.gov/dpdx/)

Multiple families of trematodes cause intestinal infections, and most of them are found in Asia. The Brachylaimidae family can be found in Oceania. The families found in Africa include Echinostomatidae, Gastrodiscidae, Heterophyidae, and Paramphistomidae. Those that have been reported in Europe include Echinostomatidae, Gastrodiscidae, Heterophyidae, and Nanophyetidae. A minority are present in the Americas, particularly Heterophyidae and Paramphistomidae.^[4]

The largest human outbreaks of Fasciola species infection have occurred in the Gilan Province of Iran, affecting more than 15,000 people.^[28]

Bihar, East India, was recently found to be endemic for fasciolopsiasis, especially since this area is generally poor, with both villagers and local medical practitioners lacking awareness about the parasite.^[29]

China, Japan, and South Korea are considered high prevalence areas for human E hortense infections. This is especially true in Koje-myon, Kochang-gun, Kyongsangnam-do Province of South Korea, where prevalence has been reported to be up to 9.5%.^[30]

In Xieng Khouang Province, Lao PDR (a country close to Myanmar), Cambodia, China, Thailand, and Vietnam, the rate of positivity for small trematode eggs was 4.4%, including O viverrini, heterophyids, and lecithodendriids.^[31]

In 2017, Tanzania reported their first case of E ilocanum infection after ingestion of raw fish (Tanganyika perch and Emperor Cichlid ”yellow belly”) caught from Lake Tanganyika by a group of travelers.^[32]

Parasitism with heterophyids are mostly due to Heterophyes and Metagonimus. An extensive review by Hung et al showed a worldwide distribution of heterophyid species, with most human infections reported in Egypt and East Asia.^[33]

In Boseong River, Gokseong-gun, South Korea, it has been shown that the eggs of M yokogawai and other Metagonimus species could be found in 24.3% of residents.^[34]

In Tabiz, Iran, vegetable contamination (tarragon, mint) with heterophyid eggs has been reported, providing other potential sources of infection with these parasites.^[35]

G seoi is endemic to Shinan-gun, Jeollanam-do, Korea, based on surveillance of oysters in 1996.^[36]A 2017 report showed that 100% of oysters sampled from Shinan-gun were infected with G seoi metacercaria.^[37]

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. These intestinal infections are important public health problems, particularly among school children in developing countries.^[38]

Prognosis

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

Immunocompromised hosts may be at an increased risk of complications. For example, G seoi worms were found to penetrate into colonic lymphoid tissue in a patient with colon cancer.^[39]

Patient Education

Health education is essential. Instruct patients on proper food preparation to avoid infection with intestinal flukes. Proper washing and thorough cooking of vegetables or fish are essential to prevent egg ingestion. 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.

Clinical Presentation

Chai JY, Jung BK. General overview of the current status of human foodborne trematodiasis. Parasitology. 2022 Sep. 149 (10):1262-1285. [QxMD MEDLINE Link]. [Full Text].
Toledo R, Álvarez-Izquierdo M, Esteban JG, Muñoz-Antoli C. Neglected food-borne trematodiases: echinostomiasis and gastrodiscoidiasis. Parasitology. 2022 Sep. 149 (10):1319-1326. [QxMD MEDLINE Link]. [Full Text].
Neglected Tropical Diseases. World Health Organization. Available at http://www.who.int/neglected_diseases/diseases/en/.
Toledo R, Munoz-Antoli C, Esteban JG. Intestinal Trematode Infections. Toledo R, Fried B. Digenetic Trematodes, Advances in Experimental Medicine and Biology. New York: Springer Science+Business Media; 2014. 766: 201-240.
Chai JY, Shin EH, Lee SH, Rim HJ. Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol. 2009 Oct. 47 Suppl:S69-102. [QxMD MEDLINE Link]. [Full Text].
Fürst T, Sayasone S, Odermatt P, Keiser J, Utzinger J. Manifestation, diagnosis, and management of foodborne trematodiasis. BMJ. 2012 Jun 26. 344:e4093. [QxMD MEDLINE Link].
Toledo R, Esteban JG, Fried B. Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis. 2012 Aug. 31 (8):1705-18. [QxMD MEDLINE Link].
Biswal DK, Ghatani S, Shylla JA, Sahu R, Mullapudi N, Bhattacharya A, et al. An integrated pipeline for next generation sequencing and annotation of the complete mitochondrial genome of the giant intestinal fluke, Fasciolopsis buski (Lankester, 1857) Looss, 1899. PeerJ. 2013 Nov 12. 1:e207. [QxMD MEDLINE Link]. [Full Text].
Toledo R, Esteban JG. An update on human echinostomiasis. Trans R Soc Trop Med Hyg. 2016 Jan. 110 (1):37-45. [QxMD MEDLINE Link].
Kumar V. The digenetic trematodes, Fasciolopsis buski, Gastrodiscoides hominis and Artyfechinostomum malayanum, as zoonotic infections in South Asian countries. Ann Soc Belg Med Trop. 1980 Dec. 60(4):331-9. [QxMD MEDLINE Link].
Seo M, Shin DH, Guk SM, Oh CS, Lee EJ, Shin MH, et al. Gymnophalloides seoi eggs from the stool of a 17th century female mummy found in Hadong, Republic of Korea. J Parasitol. 2008 Apr. 94(2):467-72. [QxMD MEDLINE Link].
Bhattacharjee HK, Yadav D, Bagga D. Fasciolopsiasis presenting as intestinal perforation: a case report. Trop Gastroenterol. 2009 Jan-Mar. 30(1):40-1. [QxMD MEDLINE Link].
Chai JY. Echinotomes in humans. Fried B, Toledo R, eds. The Biology of Echinostomes. New York, NY: Springer; 2009.
Toledo R, Esteban JG, Fried B. Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol. 2006. 63:285-365. [QxMD MEDLINE Link].
Cho YK, Ryang YS, Kim IS, Park SK, Im JA, Lee KJ. Differential immune profiles following experimental Echinostoma hortense infection in BALB/c and C3H/HeN mice. Parasitol Res. 2007 Apr. 100(5):1053-61. [QxMD MEDLINE Link].
Sotillo J, Muñoz-Antoli C, Marcilla A, Fried B, Guillermo Esteban J, Toledo R. Echinostoma caproni: kinetics of IgM, IgA and IgG subclasses in the serum and intestine of experimentally infected rats and mice. Exp Parasitol. 2007 Aug. 116(4):390-8. [QxMD MEDLINE Link].
Cortés A, Muñoz-Antoli C, Martín-Grau C, Esteban JG, Grencis RK, Toledo R. Differential alterations in the small intestine epithelial cell turnover during acute and chronic infection with Echinostoma caproni (Trematoda). Parasit Vectors. 2015 Jun 18. 8:334. [QxMD MEDLINE Link].
Lee JJ, Kim HJ, Kim MJ, Yi Lee JW, Jung BK, Lee JY. Decrease of Metagonimus yokogawai endemicity along the Tamjin River basin. Korean J Parasitol. 2008 Dec. 46(4):289-91. [QxMD MEDLINE Link]. [Full Text].
Yu JR, Chung JS, Huh S, Lee SH, Chai JY. PCR-RFLP pattern of three kinds of Metagonimus in Korea. Korean J Parasitol. 1997 Dec. 35(4):271-6. [QxMD MEDLINE Link].
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. [QxMD MEDLINE Link].
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. 1980 Dec. 11(4):559-65. [QxMD MEDLINE Link].
Chandra SS. Epidemiology of Fasciolopsis buski in Uttar Pradesh. Indian J Med Res. 1984 Jan. 79:55-9. [QxMD MEDLINE Link].
Gilman RH, Mondal G, Maksud M. Endemic focus of Fasciolopsis buski infection in Bangladesh. Am J Trop Med Hyg. 1982 Jul. 31(4):796-802. [QxMD MEDLINE Link].
Hadidjaja P, Dahri HM, Roesin R. First autochthonous case of Fasciolopsis buski infection in Indonesia. Am J Trop Med Hyg. 1982 Sep. 31(5):1065. [QxMD MEDLINE Link].
Lo CT, Lee KM. Intestinal parasites among the Southeast Asian laborers in Taiwan during 1993-1994. Zhonghua Yi Xue Za Zhi (Taipei). 1996 Jun. 57(6):401-4. [QxMD MEDLINE Link].
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. [QxMD MEDLINE Link].
Rowel C, Fred B, Betson M, Sousa-Figueiredo JC, Kabatereine NB, Stothard JR. Environmental epidemiology of intestinal schistosomiasis in Uganda: population dynamics of biomphalaria (gastropoda: planorbidae) in Lake Albert and Lake Victoria with observations on natural infections with digenetic trematodes. Biomed Res Int. 2015. 2015:717261. [QxMD MEDLINE Link].
Ashrafi K, Saadat F, O'Neill S, Rahmati B, Amin Tahmasbi H, Pius Dalton J, et al. The Endemicity of Human Fascioliasis in Guilan Province, Northern Iran: the Baseline for Implementation of Control Strategies. Iran J Public Health. 2015 Apr. 44 (4):501-11. [QxMD MEDLINE Link].
Achra A, Prakash P, Shankar R. Fasciolopsiasis: Endemic focus of a neglected parasitic disease in Bihar. Indian J Med Microbiol. 2015 Jul-Sep. 33 (3):364-8. [QxMD MEDLINE Link].
Liu ZX, Zhang Y, Liu YT, Chang QC, Su X, Fu X, et al. Complete Mitochondrial Genome of Echinostoma hortense (Digenea: Echinostomatidae). Korean J Parasitol. 2016 Apr. 54 (2):173-9. [QxMD MEDLINE Link].
Chai JY, Sohn WM, Jung BK, Yong TS, Eom KS, Min DY, et al. Intestinal Helminths Recovered from Humans in Xieng Khouang Province, Lao PDR with a Particular Note on Haplorchis pumilio Infection. Korean J Parasitol. 2015 Aug. 53 (4):439-45. [QxMD MEDLINE Link].
Chunge RN, Chunge CN. Infection with Echinostoma sp. in a group of travellers to Lake Tanganyika, Tanzania, in January 2017. J Travel Med. 2017 Sep 1. 24 (5):[QxMD MEDLINE Link].
Hung NM, Madsen H, Fried B. Global status of fish-borne zoonotic trematodiasis in humans. Acta Parasitol. 2013 Sep. 58 (3):231-58. [QxMD MEDLINE Link].
Chai JY, Jung BK, Kim DG, Kim JL, Lim H, Shin EH, et al. Heterophyid trematodes recovered from people residing along the Boseong River, South Korea. Acta Trop. 2015 Aug. 148:142-6. [QxMD MEDLINE Link].
Balarak D, Ebrahimi M, Modrek MJ, Bazrafshan E, Mahvi AH, Mahdavi Y. Investigation of Parasitic Contaminations of Vegetables Sold in Markets in the City of Tabriz in 2014. Glob J Health Sci. 2016 Oct 1. 8 (10):54811. [QxMD MEDLINE Link].
Lee SH, Sohn WM, Hong SJ, Huh S, Seo M, Choi MH, et al. A nationwide survey of naturally produced oysters for infection with Gymnophalloides seoi metacercariae. Korean J Parasitol. 1996 Jun. 34 (2):107-12. [QxMD MEDLINE Link].
Sohn WM, Na BK, Cho SH, Lee WJ. Prevalence and Density of Digenetic Trematode Metacercariae in Clams and Oysters from Western Coastal Regions of the Republic of Korea. Korean J Parasitol. 2017 Aug. 55 (4):399-408. [QxMD MEDLINE Link].
Jejaw A, Zemene E, Alemu Y, Mengistie Z. High prevalence of Schistosoma mansoni and other intestinal parasites among elementary school children in Southwest Ethiopia: a cross-sectional study. BMC Public Health. 2015 Jul 2. 15:600. [QxMD MEDLINE Link].
Seo M, Chun H, Ahn G, Jang KT, Guk SM, Chai JY. A case of colonic lymphoid tissue invasion by Gymnophalloides seoi in a Korean man. Korean J Parasitol. 2006 Mar. 44(1):87-9. [QxMD MEDLINE Link]. [Full Text].
Belizario VY, De Leon WU. Medical parasitology in the Philippines. University of the Philippines Press; 2015.
Doanh PN, Nawa Y. Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Trans R Soc Trop Med Hyg. 2016 Jan. 110 (1):13-20. [QxMD MEDLINE Link].
Tribble D, Wagner KF. Trematode infections. Infectious Disease Practice. 1996. 20:69-73.
Quang TD, Duong TH, Richard-Lenoble D, Odermatt P, Khammanivong K. [Emergence in humans of fascioliasis (from Fasciola gigantica) and intestinal distomatosis (from Fasciolopsis buski) in Laos]. Sante. 2008 Jul-Sep. 18(3):119-24. [QxMD MEDLINE Link].
Kajugu PE, Hanna RE, Edgar HW, McMahon C, Cooper M, Gordon A, et al. Fasciola hepatica: Specificity of a coproantigen ELISA test for diagnosis of fasciolosis in faecal samples from cattle and sheep concurrently infected with gastrointestinal nematodes, coccidians and/or rumen flukes (paramphistomes), under field conditions. Vet Parasitol. 2015 Sep 15. 212 (3-4):181-7. [QxMD MEDLINE Link].
Centers for Disease Control and Prevention (Content source: Global Health, Division of Parasitic Diseases and Malaria). Fasciola. Resources for Health Professionals. Centers for Disease Control and Prevention. Available at https://www.cdc.gov/parasites/fasciola/health_professionals/index.html. Page last reviewed: September 16, 2020; Accessed: August 29, 2023.
Worasith C, Kamamia C, Yakovleva A, Duenngai K, Wangboon C, Sithithaworn J, et al. Advances in the Diagnosis of Human Opisthorchiasis: Development of Opisthorchis viverrini Antigen Detection in Urine. PLoS Negl Trop Dis. 2015 Oct. 9 (10):e0004157. [QxMD MEDLINE Link].
Teimoori S, Arimatsu Y, Laha T, Kaewkes S, Sereerak P, Sripa M, et al. Chicken IgY-based coproantigen capture ELISA for diagnosis of human opisthorchiasis. Parasitol Int. 2016 Apr 29. [QxMD MEDLINE Link].
Centers for Disease Control and Prevention (Content source: Global Health, Division of Parasitic Diseases and Malaria). Parasites - Opisthorchis Infection. Resources for Health Professionals. Centers for Disease Control and Prevention. Available at https://www.cdc.gov/parasites/opisthorchis/health_professionals/index.html. Page last reviewed: May 26, 2020; Accessed: August 29, 2023.
Centers for Disease Control and Prevention (Page last reviewed: May 20, 2020). Parasites - Clonorchis. Resources for Health Professionals. Centers for Disease Control and Prevention. Available at https://www.cdc.gov/parasites/clonorchis/health_professionals/index.html. Page last reviewed: May 20, 2020; Accessed: August 29, 2023.
Centers for Disease Control and Prevention (Content source: Global Health, Division of Parasitic Diseases and Malaria). Metagonimiasis (DPDx - Laboratory Identification of Parasites of Public Health Concern). Centers for Disease Control and Prevention. Available at https://www.cdc.gov/dpdx/metagonimiasis/index.html. Page last reviewed: December 29, 2017; Accessed: August 29, 2023.
Centers for Disease Control and Prevention (Content source: Global Health, Division of Parasitic Diseases and Malaria). Heterophyiasis (DPDx - Laboratory Identification of Parasites of Public Health Concern). Centers for Disease Control and Prevention. Available at https://www.cdc.gov/dpdx/heterophyiasis/index.html. Page last reviewed: January 3, 2018; Accessed: August 29, 2023.
Centers for Disease Control and Prevention (Content source: Global Health, Division of Parasitic Diseases and Malaria). Echinostomiasis (DPDx - Laboratory Identification of Parasites of Public Health Concern). Centers for Disease Control and Prevention. Available at https://www.cdc.gov/dpdx/echinostomiasis/index.html. Page last reviewed: June 25, 2019; Accessed: August 29, 2023.
Sapero JJ, Lawless DK. The MIF stain-preservation technic for the identification of intestinal protozoa. Am J Trop Med Hyg. 1953 Jul. 2(4):613-9. [QxMD MEDLINE Link]. [Full Text].
Price DL. Comparison of three collection-preservation methods for detection of intestinal parasites. J Clin Microbiol. 1981 Dec. 14(6):656-60. [QxMD MEDLINE Link]. [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. [QxMD MEDLINE Link].
Jeon HK, Lee D, Park H, Min DY, Rim HJ, Zhang H, et al. Human infections with liver and minute intestinal flukes in Guangxi, China: analysis by DNA sequencing, ultrasonography, and immunoaffinity chromatography. Korean J Parasitol. 2012 Dec. 50(4):391-4. [QxMD MEDLINE Link]. [Full Text].
Manpratum Y, Kaewkes W, Echaubard P, Sripa B, Kaewkes S. New locality record for Haplorchoides mehrai and possible interactions with Opisthorchis viverrini metacercariae in cyprinid fishes in Northeast Thailand. Parasitol Res. 2017 Feb. 116 (2):601-608. [QxMD MEDLINE Link].
Zheng S, Zhu Y, Zhao Z, Wu Z, Okanurak K, Lv Z. Liver fluke infection and cholangiocarcinoma: a review. Parasitol Res. 2017 Jan. 116 (1):11-19. [QxMD MEDLINE Link].
Won EJ, Kim SH, Kee SJ, Shin JH, Suh SP, Chai JY, et al. Multiplex Real-Time PCR Assay Targeting Eight Parasites Customized to the Korean Population: Potential Use for Detection in Diarrheal Stool Samples from Gastroenteritis Patients. PLoS One. 2016. 11 (11):e0166957. [QxMD MEDLINE Link].
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. 2000 Oct. 86(5):1170-2. [QxMD MEDLINE Link].
Yu JR, Chai JY. Metagonimus. Liu D, ed. Molecular Detection of Foodborne Pathogens. Boca Raton, Florida: CRC Press (Taylor & Francis Group); 2010. Ch 59.
Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I. Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis Aquat Organ. 2004 Apr 21. 59(1):35-41. [QxMD MEDLINE Link].
Kumchoo K, Wongsawad C, Vanittanakom P, Chai JY, Rojanapaibul A. Effect of niclosamide on the tegumental surface of Haplorchis taichui using scanning electron microscopy. J Helminthol. 2007 Dec. 81(4):329-37. [QxMD MEDLINE Link].
Kolenyak-Santos F, Garnero C, de Oliveira RN, de Souza AL, Chorilli M, Allegretti SM, et al. Nanostructured Lipid Carriers as a Strategy to Improve the In Vitro Schistosomiasis Activity of Praziquantel. J Nanosci Nanotechnol. 2015 Jan. 15 (1):761-72. [QxMD MEDLINE Link].
Lam NS, Long X, Su XZ, Lu F. Artemisinin and its derivatives in treating helminthic infections beyond schistosomiasis. Pharmacol Res. 2018 Jul. 133:77-100. [QxMD MEDLINE Link].
Souza JG, Lopes Torres EJ, Garcia JS, Gomes AP, Rodrigues-Silva R, Maldonado A Jr, et al. Light and scanning electron microscopy study of in vitro effects of artesunate in newly excysted metacercariae of Echinostoma paraensei (Trematoda: Digenea). Exp Parasitol. 2017 Mar. 174:10-16. [QxMD MEDLINE Link].
Egaten (triclabendazole) [package insert]. East Hanover, NJ: Novartis Pharmaceuticals, Corp. February, 2019. Available at [Full Text].
Centers for Disease Control and Prevention. Fasciola – Resources for Health Professionals. CDC. Available at https://www.cdc.gov/parasites/fasciola/health_professionals/index.html#Treatment. 2019 Jan 14; Accessed: 2019 Feb 19.
Soukhathammavong P, Odermatt P, Sayasone S, et al. Efficacy and safety of mefloquine, artesunate, mefloquine-artesunate, tribendimidine, and praziquantel in patients with Opisthorchis viverrini: a randomised, exploratory, open-label, phase 2 trial. Lancet Infect Dis. 2011 Feb. 11(2):110-8. [QxMD MEDLINE Link].
Foodborne trematodiasis. World Health Organization. Available at http://www.who.int/mediacentre/factsheets/fs368/en/. March 2016;
Li L, Liu X, Zhou B, Zhang S, Wang G, Ma G, et al. Multiple food-borne trematodiases with profound systemic involvement: a case report and literature review. BMC Infect Dis. 2019 Jun 14. 19 (1):526. [QxMD MEDLINE Link].
WHO Study Group & World Health Organization. Control of Foodborne Trematode Infections. WHO Technical Report Series. 1995. 849:1–157.
Ohnishi K, Ainoda Y, Imamura A, Iwabuchi S, Okuda M, Nakano T. JAID/JSC Guidelines for Infection Treatment 2015-Intestinal infections. J Infect Chemother. 2018 Jan. 24 (1):1-17. [QxMD MEDLINE Link].
Worasith C, Kamamia C, Yakovleva A, Duenngai K, Wangboon C, Sithithaworn J, et al. Advances in the Diagnosis of Human Opisthorchiasis: Development of Opisthorchis viverrini Antigen Detection in Urine. PLoS Negl Trop Dis. 2015. 9 (10):e0004157. [QxMD MEDLINE Link].
McNeilly TN, Nisbet AJ. Immune modulation by helminth parasites of ruminants: implications for vaccine development and host immune competence. Parasite. 2014. 21:51. [QxMD MEDLINE Link].
Adams M, Motarjemi Y. Basic Food Safety for Health Workers. 1999.
Ahn YK. [Intestinal flukes of genus Metagonimus and their second intermediate hosts in Kangwon-do]. Korean J Parasitol. 1993 Dec. 31(4):331-40. [QxMD MEDLINE Link].
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. 1983 Jun. 14(2):216-9. [QxMD MEDLINE Link].
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. 1997 Dec. 35(4):233-8. [QxMD MEDLINE Link].
Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int. 2002 Jun. 51(2):129-54. [QxMD MEDLINE Link].
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. 1995 Sep. 33(3):219-23. [QxMD MEDLINE Link].
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. 1987 May. 36(3):586-91. [QxMD MEDLINE Link].
Eckert J. Workshop summary: food safety: meat- and fish-borne zoonoses. Vet Parasitol. 1996 Aug. 64(1-2):143-7. [QxMD MEDLINE Link].
Fernandes BJ, Cooper JD, Cullen JB, Freeman RS, Ritchie AC, Scott AA. Systemic infection with Alaria americana (Trematoda). Can Med Assoc J. 1976 Dec 4. 115(11):1111-4. [QxMD MEDLINE Link].
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. [QxMD MEDLINE Link].
Gajadhar AA, Scandrett WB, Forbes LB. Overview of food- and water-borne zoonotic parasites at the farm level. Rev Sci Tech. 2006 Aug. 25(2):595-606. [QxMD MEDLINE Link].
Graczyk TK, Fried B. Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg. 1998 Apr. 58(4):501-4. [QxMD MEDLINE Link].
Graczyk TK, Gilman RH, Fried B. Fasciolopsiasis: is it a controllable food-borne disease?. Parasitol Res. 2001 Jan. 87(1):80-3. [QxMD MEDLINE Link].
Guk SM, Park JH, Shin EH, Kim JL, Lin A, Chai JY. Prevalence of Gymnophalloides seoi infection in coastal villages of Haenam-gun and Yeongam-gun, Republic of Korea. Korean J Parasitol. 2006 Mar. 44(1):1-5. [QxMD MEDLINE Link]. [Full Text].
Harinasuta T, Bunnag D, Radomyos P. Efficacy of praziquantel on fasciolopsiasis. Arzneimittelforschung. 1984. 34(9B):1214-5. [QxMD MEDLINE Link].
Kaul BK, Singhal GD, Pillai PN. Artyfechinostomum mehrai infestation with bowel perforation. J Indian Med Assoc. 1974 Oct 16. 63(8):263-5. [QxMD MEDLINE Link].
Keiser J, Utzinger J. Food-borne trematodiases. Clin Microbiol Rev. 2009 Jul. 22(3):466-83. [QxMD MEDLINE Link]. [Full Text].
Kim DG, Kim TS, Cho SH, Song HJ, Sohn WM. Heterophyid metacercarial infections in brackish water fishes from Jinju-man (Bay), Kyongsangnam-do, Korea. Korean J Parasitol. 2006 Mar. 44(1):7-13. [QxMD MEDLINE Link]. [Full Text].
Leung TL, Poulin R, Keeney DB. Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp. Int J Parasitol. 2009 Feb. 39(3):327-31. [QxMD MEDLINE Link].
Liu LX, Harinasuta KT. Liver and intestinal flukes. Gastroenterol Clin North Am. 1996 Sep. 25(3):627-36. [QxMD MEDLINE Link].
Maclean JD, Cross J, Mahanty S. Liver, lung, and intestinal fluke infections. 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. 1985 Mar. 59(1):19-22. [QxMD MEDLINE Link].
Manjarumkar PV, Shah PM. Epidemiological study of Fasciolopsis Buski in Palghar Taluk. Indian J Public Health. 1972 Jan. 16(1):3-6. [QxMD MEDLINE Link].
Manning GS, Ratanarat C. Fasciolopsis buski (Lankester, 1857) in Thailand. Am J Trop Med Hyg. 1970 Jul. 19(4):613-9. [QxMD MEDLINE Link].
Mas-Coma S, Valero MA, Bargues MD. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol. 2009. 69:41-146. [QxMD MEDLINE Link].
McDonald HR, Kazacos KR, Schatz H, Johnson RN. Two cases of intraocular infection with Alaria mesocercaria (Trematoda). Am J Ophthalmol. 1994 Apr 15. 117(4):447-55. [QxMD MEDLINE Link].
Muttalib MA, Islam N. Fasciolopsis buski in Bangladesh-a pilot study. J Trop Med Hyg. 1975 Jun. 78(6):135-7. [QxMD MEDLINE Link].
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. 2007 Mar. 45(1):33-8. [QxMD MEDLINE Link]. [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. [QxMD MEDLINE Link].
Pungpak S, Radomyos P, Radomyos BE. Treatment of Opisthorchis viverrini and intestinal fluke infections with Praziquantel. Southeast Asian J Trop Med Public Health. 1998 Jun. 29(2):246-9. [QxMD MEDLINE Link].
Radomyos B, Wongsaroj T, Wilairatana P. Opisthorchiasis and intestinal fluke infections in northern Thailand. Southeast Asian J Trop Med Public Health. 1998 Mar. 29(1):123-7. [QxMD MEDLINE Link].
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. 1994 Jun. 45(2):133-5. [QxMD MEDLINE Link].
Shah PM, Udani PM, Manjarumkar PV. Fasciolopsis Buski infestation in children. Indian Pediatr. 1973 Dec. 10(12):721-4. [QxMD MEDLINE Link].
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. 1974 Dec. 5(4):556-9. [QxMD MEDLINE Link].
Taraschewski H, Mehlhorn H, Bunnag D. Effects of praziquantel on human intestinal flukes (Fasciolopsis buski and Heterophyes heterophyes). Zentralbl Bakteriol Mikrobiol Hyg [A]. 1986 Nov. 262(4):542-50. [QxMD MEDLINE Link].
Waikagul J. Intestinal fluke infections in Southeast Asia. Southeast Asian J Trop Med Public Health. 1991 Dec. 22 Suppl:158-62. [QxMD MEDLINE Link].
Wegner DH. The profile of the trematodicidal compound praziquantel. Arzneimittelforschung. 1984. 34(9B):1132-6. [QxMD MEDLINE Link].
Wiwanitkit V, Nithiuthai S, Suwansaksri J. Motility of minute intestinal fluke, Haplorchinae spp, metacercariae in fish dishes prepared by different uncooked methods. MedGenMed. 2002 Mar 6. 4(1):8. [QxMD MEDLINE Link].
Wiwanitkit V, Suwansaksri J, Chaiyakhun Y. High prevalence of Fasciolopsis buski in an endemic area of liver fluke infection in Thailand. MedGenMed. 2002 Jul 9. 4(3):6. [QxMD MEDLINE Link].

Media Gallery

Life cycle of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.
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.
Egg of Fasciolopsis buski. Images reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.
Adult fluke of Fasciolopsis buski. Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.
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.
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.
Various animals may be definitive hosts for different Echinostoma species, such as aquatic birds, carnivores, rodents, and humans. Unembryonated eggs are passed in stool (1), and development occurs in the water (2). The miracidium takes an average of 10 days to mature and then hatches (3), penetrating the first intermediate host, a snail (4). Snails, in general, serve as the first intermediate host. The intramolluscan stages are as follows: sporocyst (4a); rediae (4b); and cercariae (4c). Cercariae may then encyst as metacercariae in the same first intermediate host or leave to penetrate a new second intermediate host (5). Several animals may become the second intermediate host, such as other snails, bivalves, fish, and tadpoles. The definitive host gets infected after eating infected second intermediate hosts (6). The metacercariae excyst in the duodenum (7). Adults then live in the small intestine (8). Image reproduced from the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, GA.
Magnified image of Echinostoma spp. egg. Echinostoma eggs resemble F busk and Fasciola eggs, with the latter two only bigger in size. Specimen slides courtesy of the University of the Philippines - College of Public Health, Department of Parasitology.
Low power magnification (arrow) of a Heterophyid egg. Specimen slides courtesy of the University of the Philippines - College of Public Health, Department of Parasitology.
Magnified view of a Heterophyid egg. Specimen slides courtesy of the University of the Philippines - College of Public Health, Department of Parasitology.

of 10

Table 1. Common Intestinal Trematode Infections

Infection	Source*	Geographic Distribution**
Fasciolopsiasis	Freshwater plants (water caltrop, water chestnut)	Asia and Indian subcontinent, especially in areas where humans raise pigs and consume freshwater plants (as of December 8, 2017)
Echinostomiasis	Tadpoles, freshwater snails, fish, frogs	Worldwide, but human cases seen most frequently in Southeast Asia and in areas where undercooked or raw freshwater snails, clams, and fish are eaten (as of December 27, 2017)
Heterophyiasis	Fish	Egypt, Middle East, Far East (as of January 3, 2018)
Metagonimiasis	Fish (cyprinid)	Far East, Siberia, Manchuria, the Balkan states, Israel, Spain (as of December 29, 2017)
* Adapted with permission from Tribble D, Wagner KF. Trematode infections. Infectious Disease Practice. 1996; 20:69-73. ** Updated data from the Centers for Disease Control and Prevention (DPDx Laboratory Identification of Parasites of Public Health Concern. Available: http://www.cdc.gov/dpdx/)

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

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.

Back to List

Author

Joseph Adrian L Buensalido, MD Clinical Associate Professor, Division of Infectious Diseases, Department of Medicine, Philippine General Hospital, University of the Philippines Manila College of Medicine; Specialist in Infectious Diseases, Private Practice

Joseph Adrian L Buensalido, MD is a member of the following medical societies: American Society for Microbiology, Infectious Diseases Society of America, Michigan Infectious Disease Society, Philippine College of Physicians, Philippine Medical Association, Philippine Society for Microbiology and Infectious Diseases

Disclosure: Serve(d) as a speaker or a member of a speakers bureau for: Unilab; BSV Bioscience; Philcare Pharma<br/>Received sponsorship to medical conference for: Pfizer; Natrapharm.

Coauthor(s)

Marja Arcangel Bernardo-Buensalido, MD Infectious Diseases Specialist, Section of Infectious Diseases, Department of Medicine, University of the Philippines-Philippine General Hospital

Marja Arcangel Bernardo-Buensalido, MD is a member of the following medical societies: Philippine College of Physicians

Disclosure: Nothing to disclose.

Specialty Editor Board

Francisco Talavera, PharmD, PhD Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Received salary from Medscape for employment. for: Medscape.

Chief Editor

Michael Stuart Bronze, MD David Ross Boyd Professor and Chairman, Department of Medicine, Stewart G Wolf Endowed Chair in Internal Medicine, Department of Medicine, University of Oklahoma Health Science Center; Master of the American College of Physicians; Fellow, Infectious Diseases Society of America; Fellow of the Royal College of Physicians, London

Michael Stuart Bronze, MD is a member of the following medical societies: Alpha Omega Alpha, American College of Physicians, American Medical Association, Association of Professors of Medicine, Infectious Diseases Society of America, Oklahoma State Medical Association, Southern Society for Clinical Investigation

Disclosure: Nothing to disclose.

Additional Contributors

Chi Hiong U Go, MD Assistant Professor, Department of Internal Medicine, Texas Tech University Health Science Center at Odessa

Chi Hiong U Go, MD is a member of the following medical societies: American College of Physicians-American Society of Internal Medicine

Disclosure: Nothing to disclose.

Thomas E Herchline, MD Professor of Medicine, Wright State University, Boonshoft School of Medicine; Medical Consultant, Public Health, Dayton and Montgomery County (Ohio) Tuberculosis Clinic

Thomas E Herchline, MD is a member of the following medical societies: Alpha Omega Alpha, Infectious Diseases Society of America, Infectious Diseases Society of Ohio

Disclosure: Received research grant from: Regeneron.

Burke A Cunha, MD Professor of Medicine, State University of New York School of Medicine at Stony Brook; Chief, Infectious Disease Division, Winthrop-University Hospital

Burke A Cunha, MD is a member of the following medical societies: American College of Chest Physicians, American College of Physicians, Infectious Diseases Society of America

Disclosure: Nothing to disclose.

Asim A Jani, MD, MPH, FACP Clinician-Educator and Epidemiologist, Consultant and Senior Physician, Florida Department of Health; Diplomate, Infectious Diseases, Internal Medicine and Preventive Medicine

Asim A Jani, MD, MPH, FACP is a member of the following medical societies: American Association of Public Health Physicians, American College of Physicians, American College of Preventive Medicine, American Medical Association, American Public Health Association, Infectious Diseases Society of America

Disclosure: Nothing to disclose.

Paul Chen University of Texas Southwestern Medical School

Disclosure: Nothing to disclose.

Anna Flor G Malundo, MD, FPCP Medical Specialist in STD/AIDS Guidance, Intervention and Prevention (SAGIP) Clinic, Section of Infectious Diseases, Department of Medicine, Philippine General Hospital, University of the Philippines Manila College of Medicine, Philippines

Anna Flor G Malundo, MD, FPCP is a member of the following medical societies: Philippine College of Physicians, Philippine Society for Microbiology and Infectious Diseases

Disclosure: Nothing to disclose.

Acknowledgements

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.