Trematoda

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Trematoda
Botulus microporus.jpg
Botulus microporus, a giant digenean parasite from the intestine of a lancetfish
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Platyhelminthes
Superclass: Neodermata
Class: Trematoda
Rudolphi, 1808
Subclasses

Trematoda is a class of flatworms known as flukes or trematodes. They are obligate internal parasites with a complex life cycle requiring at least two hosts. The intermediate host, in which asexual reproduction occurs, is usually a snail. The definitive host, where the flukes sexually reproduce, is a vertebrate. Infection by trematodes can cause disease in all five traditional vertebrate classes: mammals, birds, amphibians, reptiles, and fish.

Contents

Etymology

Trematodes are commonly referred to as flukes. This term can be traced back to the Old English name for flounder, and refers to the flattened, rhomboidal shape of the organisms.

Taxonomy

There are 18,000 [1] to 24,000 [2] known species of trematodes, divided into two subclasses — the Aspidogastrea and the Digenea. Aspidogastrea is the smaller subclass, comprising 61 species. These flukes mainly infect bivalves and bony fishes. [3] Digenea — which comprise the majority of trematodes — are found in certain mollusks and vertebrates.

Trematodes of medical importance

Flukes that cause disease in humans are often classified based on the organ system they infect. For example:

Anatomy

Various trematodes, from 1911 Encyclopaedia Britannica TrematodesFig9 EncBrit1911.png
Various trematodes, from 1911 Encyclopædia Britannica

Trematodes are flattened oval or worm-like animals, usually no more than a few centimeters in length, although species as small as 1 millimetre (0.039 in) are known. Their most distinctive external feature is the presence of two suckers, one close to the mouth, and the other on the underside of the animal. [12]

The body surface of trematodes comprises a tough syncytial tegument, which helps protect against digestive enzymes in those species that inhabit the gut of larger animals. It is also the surface of gas exchange; there are no respiratory organs. [12]

The mouth is located at the forward end of the animal, and opens into a muscular, pumping pharynx. The pharynx connects, via a short oesophagus, to one or two blind-ending caeca, which occupy most of the length of the body. In some species, the caeca are themselves branched. As in other flatworms, there is no anus, and waste material must be egested through the mouth. [12]

Although the excretion of nitrogenous waste occurs mostly through the tegument, trematodes do possess an excretory system, which is instead mainly concerned with osmoregulation. This consists of two or more protonephridia, with those on each side of the body opening into a collecting duct. The two collecting ducts typically meet up at a single bladder, opening to the exterior through one or two pores near the posterior end of the animal. [12]

The brain consists of a pair of ganglia in the head region, from which two or three pairs of nerve cords run down the length of the body. The nerve cords running along the ventral surface are always the largest, while the dorsal cords are present only in the Aspidogastrea. Trematodes generally lack any specialized sense organs, although some ectoparasitic species do possess one or two pairs of simple ocelli. [12]

Body wall musculature: Formed of three different muscle layers: circular, longitudinal, and diagonal. The outermost layer is formed by the circular muscle fibers, directly behind that are the longitudinal muscle fibers. The inner layer is formed by the diagonal muscle fibers. Together these muscle fibers form the segmented body wall of trematodes. [13]

Oral sucker and acetabulum: In some species of Trematoda, such as T. bragai, there is an acetabulum. This saucer-shaped organ is attached to the oral sucker in some Trematodes and other parasitic worms. This allows for parasitic worms to attach to their host by penetrating the host’s tissue with spines lining the acetabulum organ. In trematodes, the oral sucker is linked to the pharynx via a canal composed of meridional, equatorial, and radial muscle fibers. [13] Together, the mouth, pharynx, and esophagus form the foregut in Trematodes. [14]

Reproductive system of blood flukes

Most trematodes are hermaphrodites, as are many internal parasites. Blood flukes (Schistosoma) are the only form of trematodes that are dioecious (have both a male and female sex). Blood flukes are unique in the way that they can undergo both asexual and sexual reproduction. Asexual reproduction occurs in the hepatopancreas of a freshwater snail, which serves as an intermediate host. Sexual reproduction occurs later in the life cycle, in the definitive (vertebrate) host.

The male reproductive system usually includes two testes, though some species may have more. The testes are located posterior and dorsal to the ventral sucker. Spermatogenesis produces biflagellate sperm (sperm with two tails). Sperm is stored in the seminal vesicles, which are connected to the testes by the vas deferens. The male reproductive system varies considerably in structure between species; this can be very useful in species identification.

The female reproductive system consists of one ovary connected to an elongated uterus by a ciliated oviduct. The uterus opens to the exterior at the genital pore (the common external opening of the male and female reproductive systems). The location of the ovary varies among different species, making the female reproductive system useful in species identification. At the base of the oviduct is a copulatory duct — termed Laurer's canal — which is analogous to a vagina. Oocytes are released from the ovary into the oocapt (the dilated proximal end of the oviduct). Sperm cells travel from the seminal vesicles through the uterus to reach the ootype (the dilated distal part of the oviduct), where fertilization occurs. The ootype is connected via a pair of ducts to a number of vitelline ducts that produce yolk. After the egg is surrounded by yolk, its shell is formed from the secretions of Mehlis' glands , the ducts of which also open into the ootype. From the ootype, the fertilized egg then travels back into the uterus, and is ultimately released from the genital atrium. [15]

Life cycles

Trematodes have a very complex life cycle and depending on what taxa they belong to, their life cycles can be completed with as little as one host compared to the typical three hosts.  When there is one host, this is normally a specific species of snail of the family Lymnaeidae. Almost all trematodes infect molluscs as the first host in the life cycle, and most have a complex life cycle involving other hosts. Most trematodes are monoecious and alternately reproduce sexually and asexually. The two main exceptions to this are the Aspidogastrea, which have no asexual reproduction, and the schistosomes, which are dioecious.

In the definitive host, in which sexual reproduction occurs, eggs are commonly shed along with host feces. Eggs shed in water release free-swimming larval forms (Miracidia) that are infective to the intermediate host, in which asexual reproduction occurs.

A species that exemplifies the remarkable life history of the trematodes is the bird fluke, Leucochloridium paradoxum . The definitive hosts, in which the parasite reproduces, are various woodland birds, while the hosts in which the parasite multiplies (intermediate host) are various species of snail. The adult parasite in the bird's gut produces eggs and these eventually end up on the ground in the bird's feces. Some eggs may be swallowed by a snail and hatch into larvae (miracidia). These larvae grow and take on a sac-like appearance. This stage is known as the sporocyst and it forms a central body in the snail's digestive gland that extends into a brood sac in the snail's head, muscular foot and eye-stalks. It is in the central body of the sporocyst where the parasite replicates itself, producing many tiny embryos (redia). These embryos move to the brood sac and mature into cercaria.

Life cycle adaptations

Trematodes have a large variation of forms throughout their life cycles. Individual trematode parasites life cycles may vary from this list. They have five larval stages along with the cystic and fully matured adult phases.

  1. Trematodes are released from the definitive host as eggs, which have evolved to withstand the harsh environment
  2. Released from the egg which hatches into the miracidium. This infects the first intermediate host in one of two ways, either active or passive transmission. The first host is normally a mollusk. a) Active transmission has adapted for dispersal in space as a free swimming ciliated miracidium with adaptations for recognizing and penetrating the first intermediate host. b) Passive transmission has adapted for dispersal in time and infects the first intermediate host contained within the egg.
  3. The sporocyst forms inside the snail first intermediate host and feeds through diffusion across the tegument.
  4. The rediae also forms inside the snail first intermediate host and feeds through a developed pharynx. Either the rediae or the sporocyst develops into the cercariae through polyembryony in the snail.
  5. The cercariae are adapted for dispersal in space and exhibit a large variety in morphology. They are adapted to recognize and penetrate the second intermediate host, and contain behavioral and physiological adaptations not present in earlier life stages.
  6. The metacercariae are an adapted cystic form dormant in the secondary intermediate host.
  7. The adult is the fully developed form which infects the definitive host.

The first stage is the miracidium that is triangular in shape and covered by a ciliated ectoderm which is the outermost layer of the three germ layers. The epidermis and epidemic tissues of the parasite will develop from the miracidium. They also have an anterior spin which helps them drill into the snail. The miracidium develops into the sporocyst, which is a sac-like structure, and in this sac the larvae begin to develop. The cells multiply. The rediae and cercariae develop from the larvae which are then released and encyst as metacercariae, for instance on aquatic plants. Humans as well as larger sea creatures get infected when they eat these plants.

When they infect humans, it can take 3–4 months for the metacercariae to mature into adult flukes and lay eggs.

Example: liver flukes

Liver flukes, one of the different species, are responsible for causing liver fluke disease which is also known as fasciolosis. They are hermaphroditic internal parasites. They are caused by the migration of a large number of immature flukes through the liver passageway or by adult flukes that migrate to the bile ducts. Liver flukes infect all grazing animals and infect humans when they eat raw or undercooked fish.

Like other flukes, the liver flukes need intermediate hosts and as a result, the transmission from animals to humans happens in three phases. The first phase is the infection of the snail (the first intermediate host) via feces. They complete their gestation and hatch as cercariae. They leave their snail hosts and infect fish who are their second intermediate host. Lastly, larger animals ingest the metacercariae in raw and undercooked fish. In humans or grazing animals, the metacercariae complete their life cycle and become full grown liver flukes.

Eusociality

One species of tremtaoda, Haplorchis pumilio, has evolved eusociality involving a colony of them creating a class of sterile soldiers. One fluke invades a host and establishes a colony of dozens to thousands of clones that work together to take it over. Since rival trematode species might also invade and replace them, a specialized caste of sterile soldier trematodes protects the colony. [16]

Soldiers are smaller, more mobile, and develop along a different pathway than sexually mature reproductives. One big difference is their mouthparts (pharynx), which are five times as big as those of the reproductives. They make up nearly a quarter of the volume of the soldier. These soldiers don’t have a germinal mass, can’t metamorphose to be reproductive, and are, therefore, obligately sterile.

Soldiers are readily distinguished from the immature and mature reproductive worms. Soldiers are more aggressive than reproductives, attacking heterospecific trematodes that infect their host in vitro. Interestingly, H. pumilio soldiers do not attack conspecifics from other colonies.

The soldiers are not evenly distributed throughout the host body. They’re found in the highest numbers in the basal visceral mass, where competing trematodes tend to multiply during the early phase of infection. This strategic positioning allows them to effectively defend against invaders, similar to how soldier distribution patterns are seen in other animals with defensive castes.

They "appear to be an obligately sterile physical caste, akin to that of the most advanced social insects". [16] Reflecting on their use for understanding the evolution of animal social castes, one review commented, "trematodes are a lineage for sociobiologists to keep a careful watch on!" [17]

Infections

Trematodes can cause disease in many types of vertebrates, including mammals, birds, reptiles, and fish. Cattle and sheep can become infected by eating contaminated food. These infections lead to a reduction in milk or meat production, which can be of significant economic importance to the livestock industry. [14]

Human trematode infections are most common in Asia, Africa and Latin America. However, trematodes can be found anywhere where untreated human waste is used as fertilizer. Humans can be infected by trematodes by immersion in or ingestion of contaminated water, or by consuming raw or undercooked contaminated animals or plants. [18]

Treatment

Albendazole can be used to treat clonorchiasis and opisthorchiasis. Triclabendazole is often used to treat fasciolosis, [19] and may also be useful in the treatment of paragonimiasis [20] and dicrocoeliasis. [21] Praziquantel is effective in the treatment of all diseases caused by flukes (clonorchiasis, dicrocoeliasis, echinostomiasis, fasciolopsiasis, fasciolosis, gastrodiscoidiasis, heterophyiasis, metagonimiasis, opisthorchiasis, paragonimiasis, and schistosomiasis). [22]

Related Research Articles

<i>Clonorchis sinensis</i> Species of fluke

Clonorchis sinensis, the Chinese liver fluke, is a liver fluke belonging to the class Trematoda, phylum Platyhelminthes. It infects fish-eating mammals, including humans. In humans, it infects the common bile duct and gall bladder, feeding on bile. It was discovered by British physician James McConnell at the Medical College Hospital in Calcutta (Kolkata) in 1874. The first description was given by Thomas Spencer Cobbold, who named it Distoma sinense. The fluke passes its lifecycle in three different hosts, namely freshwater snail as first intermediate hosts, freshwater fish as second intermediate host, and mammals as definitive hosts.

<span class="mw-page-title-main">Digenea</span> Class of flukes

Digenea is a class of trematodes in the Platyhelminthes phylum, consisting of parasitic flatworms with a syncytial tegument and, usually, two suckers, one ventral and one oral. Adults commonly live within the digestive tract, but occur throughout the organ systems of all classes of vertebrates. Once thought to be related to the Monogenea, it is now recognised that they are closest to the Aspidogastrea and that the Monogenea are more closely allied with the Cestoda. Around 6,000 species have been described to date.

<span class="mw-page-title-main">Clonorchiasis</span> Infectious disease caused by fish parasites

Clonorchiasis is an infectious disease caused by the Chinese liver fluke and two related species. Clonorchiasis is a known risk factor for the development of cholangiocarcinoma, a neoplasm of the biliary system.

<i>Fasciola hepatica</i> Species of fluke

Fasciola hepatica, also known as the common liver fluke or sheep liver fluke, is a parasitic trematode of the class Trematoda, phylum Platyhelminthes. It infects the livers of various mammals, including humans, and is transmitted by sheep and cattle to humans all over the world. The disease caused by the fluke is called fasciolosis or fascioliasis, which is a type of helminthiasis and has been classified as a neglected tropical disease. Fasciolosis is currently classified as a plant/food-borne trematode infection, often acquired through eating the parasite's metacercariae encysted on plants. F. hepatica, which is distributed worldwide, has been known as an important parasite of sheep and cattle for decades and causes significant economic losses in these livestock species, up to £23 million in the UK alone. Because of its relatively large size and economic importance, it has been the subject of many scientific investigations and may be the best-known of any trematode species. The closest relative of Fasciola hepatica is F. gigantica. These two flukes are sister species; they share many morphological features and can mate with each other.

<i>Fasciola</i> Genus of flukes

Fasciola, commonly known as the liver fluke, is a genus of parasitic trematodes. There are three species within the genus Fasciola: Fasciola nyanzae,Fasciolahepatica and Fasciolagigantica. Fasciola hepatica and F. gigantica are known to form hybrids. Both F. hepatica and F. gigantica and their hybrids infect the liver tissue of a wide variety of mammals, including humans, in a condition known as fascioliasis. F. hepatica measures up to 30 mm by 15 mm, while F. gigantica measures up to 75 mm by 15 mm. Fasciola nyanzae is thought to exclusively infect the common hippopotamus, Hippopotamus amphibius.

<span class="mw-page-title-main">Trematode life cycle stages</span>

Trematodes are parasitic flatworms of the class Trematoda, specifically parasitic flukes with two suckers: one ventral and the other oral. Trematodes are covered by a tegument, that protects the organism from the environment by providing secretory and absorptive functions.

<i>Paragonimus westermani</i> Species of fluke

Paragonimus westermani is the most common species of lung fluke that infects humans, causing paragonimiasis. Human infections are most common in eastern Asia and in South America. Paragonimiasis may present as a sub-acute to chronic inflammatory disease of the lung. It was discovered by Dutch zoologist Coenraad Kerbert in 1878.

<i>Echinostoma</i> Genus of flukes

Echinostoma is a genus of trematodes (flukes), which can infect both humans and other animals. These intestinal flukes have a three-host life cycle with snails or other aquatic organisms as intermediate hosts, and a variety of animals, including humans, as their definitive hosts.

<i>Paragonimus</i> Genus of flukes

Paragonimus is a genus of flukes (trematodes) and is the only genus in the monotypic family Paragonimidae. Some tens of species have been described, but they are difficult to distinguish, so it is not clear how many of the named species may be synonyms. The name Paragonimus is derived from the combination of two Greek words, “para” and “gonimos”. Several of the species are known as lung flukes. In humans some of the species occur as zoonoses; the term for the condition is paragonimiasis. The first intermediate hosts of Paragonimus include at least 54 species of freshwater snails from superfamilies Cerithioidea and Rissooidea.

<span class="mw-page-title-main">Paragonimiasis</span> Medical condition

Paragonimiasis is a food-borne parasitic disease caused by several species of lung flukes belonging to genus Paragonimus. Infection is acquired by eating crustaceans such as crabs and crayfishes which host the infective forms called metacercariae, or by eating raw or undercooked meat of mammals harboring the metacercariae from crustaceans.

<i>Dicrocoelium dendriticum</i> Species of fluke

Dicrocoelium dendriticum, the lancet liver fluke, is a parasite fluke that tends to live in cattle or other grazing mammals.

<span class="mw-page-title-main">Liver fluke</span> Group of liver parasites

Liver fluke is a collective name of a polyphyletic group of parasitic trematodes under the phylum Platyhelminthes. They are principally parasites of the liver of various mammals, including humans. Capable of moving along the blood circulation, they can occur also in bile ducts, gallbladder, and liver parenchyma. In these organs, they produce pathological lesions leading to parasitic diseases. They have complex life cycles requiring two or three different hosts, with free-living larval stages in water.

Metagonimoides oregonensis is a trematode, or fluke worm, in the family Heterophyidae. This North American parasite is found primarily in the intestines of raccoons, American minks, frogs in the genus Rana, and freshwater snails in the genus Goniobasis. It was first described in 1931 by E. W. Price. The parasite has a large distribution, from Oregon to North Carolina. Adult flukes vary in host range and morphology dependent on the geographical location. This results in different life cycles, as well as intermediate hosts, across the United States. On the west coast, the intermediate host is freshwater snails (Goniobasis), while on the east coast the intermediate host is salamanders (Desmognathus). The parasites on the west coast are generally much larger than on the east coast. For example, the pharynx as well as the body of the parasite are distinctly larger in Oregon than in North Carolina. The reverse pattern is observed on the east coast for uterine eggs, which are larger on the west coast. In snails, there is also a higher rate of infection in female snails than in males. Research on the life history traits of the parasites have been performed with hamsters and frogs as model species.

<i>Fasciolopsis</i> Genus of flukes

Fasciolopsis is a genus of trematodes. They are also known as giant intestinal flukes.

<i>Bucephalus polymorphus</i> Species of fluke

Bucephalus polymorphus is a type of flatworm. This species is within the Bucephalidae family of Digenea, which in turn is a subclass of Trematodes within the phylum Platyhelminthes. It is characterized by having a mouth near the middle of its body, along with a sac-like gut. The mouth opening is located in the centre of the ventral surface. This is a specific body type of cecaria known as a gastrostome.

Megalodiscus temperatus is a Digenean in the phylum Platyhelminthes. This parasite belongs to the Cladorchiidae family and is a common parasite located in the urinary bladder and rectum of frogs. The primary host is frogs and the intermediate hosts of Megalodiscus temeperatus are freshwater snails in the genus Helisoma.

<i>Alaria</i> (flatworm) Genus of flukes

Alaria is a genus of flatworms, or trematodes, in the family Diplostomidae.

<i>Metagonimus yokogawai</i> Species of fluke

Metagonimus yokogawai, or the Yokogawa fluke, is a species of a trematode, or fluke worm, in the family Heterophyidae.

Heterobilharzia is a genus of trematodes in the family Schistosomatidae. The species Heterobilharzia Americana is a parasite of the Southeastern United States and typically found in raccoons. Species of this genus are responsible for Schistosoma in canines. Cercariae found in freshwater may also cause Swimmer's itch in humans.

<span class="mw-page-title-main">Gastropod-borne parasitic disease</span> Medical condition

Gastropod-borne parasitic diseases (GPDs) are a group of infectious diseases that require a gastropod species to serve as an intermediate host for a parasitic organism that can infect humans upon ingesting the parasite or coming into contact with contaminated water sources. These diseases can cause a range of symptoms, from mild discomfort to severe, life-threatening conditions, with them being prevalent in many parts of the world, particularly in developing regions. Preventive measures such as proper sanitation and hygiene practices, avoiding contact with infected gastropods and cooking or boiling food properly can help to reduce the risk of these diseases.

References

  1. ↑ Littlewood D T J; Bray R. A. (2000). "The Digenea". Interrelationships of the Platyhelminthes. Systematics Association Special Volume. Vol. 60 (1 ed.). CRC. pp. 168–185. ISBN   978-0-7484-0903-7.
  2. ↑ Poulin, Robert; Serge Morand (2005). Parasite Biodiversity. Smithsonian. p. 216. ISBN   978-1-58834-170-9.
  3. ↑ "A Checklist of the Aspidogastrea (Platyhelminthes: Trematoda) of the World". www.biotaxa.org. Retrieved 11 June 2024.
  4. 1 2 Toledo, Rafael; Fried, Bernard, eds. (2014). Digenetic Trematodes. Advances in Experimental Medicine and Biology. Vol. 766. doi:10.1007/978-1-4939-0915-5. ISBN   978-1-4939-0914-8. ISSN   0065-2598. S2CID   28198614.
  5. ↑ Antoni, S.; Ferlay, J.; Soerjomataram, I.; Znaor, A.; Jemal, A.; Bray, F. (2017). "Bladder Cancer incidence and mortality: A global overview and recent trends". European Urology. 71 (1): 96–108. doi:10.1016/j.eururo.2016.06.010. PMID   27370177.
  6. ↑ Khurana S, Dubey ML, Malla N (April 2005). "Association of parasitic infections and cancers". Indian J Med Microbiol. 23 (2): 74–79. doi:10.1016/S0300-483X(01)00357-2. PMID   15928434.
  7. 1 2 "IARC Monographs on the Identification of Carcinogenic Hazards to Humans" . Retrieved 4 December 2022.
  8. ↑ Hughes T, O'Connor T, Techasen A, Namwat N, Loilome W, Andrews RH, Khuntikeo N, Yongvanit P, Sithithaworn P, Taylor-Robinson SD (2017). "Opisthorchiasis and cholangiocarcinoma in Southeast Asia: an unresolved problem". International Journal of General Medicine . 10: 227–237. doi: 10.2147/IJGM.S133292 . PMC   5557399 . PMID   28848361.
  9. ↑ Kaewpitoon N, Kaewpitoon SJ, Pengsaa P, Sripa B (February 2008). "Opisthorchis viverrini: the carcinogenic human liver fluke". World Journal of Gastroenterology. 14 (5): 666–74. doi: 10.3748/wjg.14.666 . PMC   2683991 . PMID   18205254.
  10. ↑ Cong, Cung-Van; Anh, Tran-Thi Tuan; Ly, Tran-Thi; Duc, Nguyen Minh (2022). "Paragonimiasis diagnosed by CT-guided transthoracic lung biopsy: Literature review and case report". Radiology Case Reports. 17 (5): 1591–1597. doi:10.1016/j.radcr.2022.02.046. ISSN   1930-0433. PMC   8927937 . PMID   35309377.
  11. ↑ "Paragonimiasis". Center for Global Health, U.S. Centers for Disease Control and Prevention (CDC). 13 October 2010. Archived from the original on 16 December 2013. Retrieved 6 September 2012.
  12. 1 2 3 4 5 Barnes, Robert D. (1982). Invertebrate Zoology. Philadelphia, PA: Holt-Saunders International. pp. 230–235. ISBN   0-03-056747-5.
  13. 1 2 D’ávila, Sthefane (18 March 2010). "Gross anatomy of the musculature and a new description of the reproductive system of Tanaisia bragai and Tanaisia inopina (Trematoda: Eucotylidae) analysed by confocal laser scanning microscopy". Acta Zoologica. 91 (2): 139–149. doi:10.1111/j.1463-6395.2008.00393.x.
  14. 1 2 Bogitsh, Burton J.; Carter, Clint E.; Oeltmann, Thomas N. (28 May 2018). Human Parasitology. Academic Press. ISBN   978-0-12-813713-0.
  15. ↑ Peoples, Robert C.; Fried, Bernard (2014). "Form and function in the Digenea". In Toledo, Rafael; Fried, Bernard (eds.). Digenetic Trematodes. Springer. pp. 14–15. ISBN   978-1-4939-0915-5.
  16. 1 2 Metz, Daniel C. G.; Hechinger, Ryan F. (30 July 2024). "The physical soldier caste of an invasive, human-infecting flatworm is morphologically extreme and obligately sterile". Proceedings of the National Academy of Sciences. 121 (31): e2400953121. Bibcode:2024PNAS..12100953M. doi:10.1073/pnas.2400953121. ISSN   0027-8424. PMC  11295071. PMID   39042696.
  17. ↑ Richards, Miriam H. (10 September 2024). "Social evolution and reproductive castes in trematode parasites". Proceedings of the National Academy of Sciences. 121 (37): e2414228121. doi:10.1073/pnas.2414228121. ISSN   0027-8424. PMC  11406270. PMID   39226370.
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  19. ↑ "Triclabendazole: MedlinePlus Drug Information".
  20. ↑ "CDC - Paragonimiasis - Resources for Health Professionals". 3 December 2021.
  21. ↑ Massoud, A.; Morsy, T. A.; Haridy, F. M. (2003). "Treatment of Egyptian dicrocoeliasis in man and animals with Mirazid". Journal of the Egyptian Society of Parasitology. 33 (2): 437–442. PMID   14964658.
  22. ↑ "Praziquantel". The American Society of Health-System Pharmacists. Archived from the original on 20 December 2016. Retrieved 8 December 2016.
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