- Author: Joseph Adrian L Buensalido, MD; Chief Editor: Michael Stuart Bronze, MD more...
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). These trematodes are included in the World Health Organization (WHO) list of neglected tropical diseases (NTDs) that prevail in tropical and subtropical conditions in 149 countries and affect more than one billion people, costing developing economies billions of dollars every year. This article focuses on intestinal trematodes, although clonorchiasis and opisthorchiasis are also discussed despite being liver fluke infections, since their respective pathogens migrate through the intestine before ending up in the liver.
Intestinal trematodes can be classified into at least 14 families (with their corresponding sources of infection found below), as follows:
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.
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 and the European Journal of Microbiology and Infectious Diseases . In the former, the species of intestinal flukes considered to be of public importance include the following:
The most common human intestinal trematode was said to be Fasciolopsis buski, which causes fasciolopsiasis, and should be differentiated from Fasciola hepatica and Fasciola gigantica, which are liver flukes that cause fascioliasis. 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. However, there are 500 species of echinostomatid flukes, with 20 species from 8 genera that can cause human infection. The genus Echinostoma is considered the largest, which includes Echinostomahortense, Echinostomaangustitestis, Echinostomacinetorchis, Echinostomaechinatum, E ilocanum, Echinostomamacrorchis, and Echinostomarevolutum.
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. Intestinal flukes have likely infected humans for hundreds of years, if not longer. Evidence of Gymnophalloides seoi infection has been traced back to the 17th century based on discovery of G seoi eggs in a Korean mummy.
See Common Intestinal Parasites, a Critical Images slideshow, to help make an accurate diagnosis.
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.
F 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 F 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.
The immature eggs (see the images below) 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 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.
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.
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.[11, 12] 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. 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.
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.
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.
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, 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.
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.
Infection with intestinal flukes affects only immigrants from endemic areas.
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. The list of countries where human trematode infections have been reported is long, with several studies indicating variable incidence rates.[16, 17, 18, 3, 19, 20, 21, 7, 22, 23, 24]
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.
The largest human outbreaks of Fasciola species infection have occurred in the Gilan Province of Iran, affecting more than 15,000 people.
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.
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.
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%.
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 Opisthorchis viverrini, heterophyids, and lecithodendriids.
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.
Intestinal flukes are endemic in Asia and in some parts of North Africa, affecting groups who live in these areas.
Intestinal flukes have no predilection for either sex.
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.
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|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.|
|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.|