Anisakis

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Anisakis
Anisakis.jpg
Anisakis simplex
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Anisakis

Dujardin, 1845
Species

Anisakis is a genus of parasitic nematodes that have lifecycles involving fish and marine mammals. [1] They are infective to humans and cause anisakiasis. People who produce immunoglobulin E in response to this parasite may subsequently have an allergic reaction, including anaphylaxis, after eating fish infected with Anisakis species.

A genus is a taxonomic rank used in the biological classification of living and fossil organisms, as well as viruses, in biology. In the hierarchy of biological classification, genus comes above species and below family. In binomial nomenclature, the genus name forms the first part of the binomial species name for each species within the genus.

Nematode phylum of animals with tubular digestive systems with openings at both ends

The nematodes or roundworms constitute the phylum Nematoda. They are a diverse animal phylum inhabiting a broad range of environments. Taxonomically, they are classified along with insects and other moulting animals in the clade Ecdysozoa, and unlike flatworms, have tubular digestive systems with openings at both ends.

Marine mammal Mammals that live in the ocean

Marine mammals are aquatic mammals that rely on the ocean and other marine ecosystems for their existence. They include animals such as seals, whales, manatees, sea otters and polar bears. They are an informal group, unified only by their reliance on marine environments for feeding.

Contents

Etymology

The genus Anisakis was defined in 1845 [2] by Félix Dujardin as a subgenus of the genus Ascaris Linnaeus, 1758. Dujardin did not make explicit the etymology, but stated that the subgenus included the species in which the males have unequal spicules ("mâles ayant des spicules inégaux"); thus, the name Anisakis is based on anis- (Greek prefix for different) and akis (Greek for spine or spicule). Two species were included in the new subgenus, Ascaris (Anisakis) distans Rudolphi, 1809 and Ascaris (Anisakis) simplex Rudolphi, 1809.

Félix Dujardin French biologist

Félix Dujardin was a French biologist born in Tours. He is remembered for his research on protozoans and other invertebrates.

<i>Ascaris</i> genus of worms

Ascaris is a genus of parasitic nematode worms known as the "small intestinal roundworms", which is a type of parasitic worm. One species, Ascaris lumbricoides, affects humans and causes the disease ascariasis. Another species, Ascaris suum, typically infects pigs. Parascaris equorum, the equine roundworm, is also commonly called an "Ascarid".

Carl Linnaeus Swedish botanist, physician, and zoologist

Carl Linnaeus, also known after his ennoblement as Carl von Linné, was a Swedish botanist, zoologist, and physician who formalised binomial nomenclature, the modern system of naming organisms. He is known as the "father of modern taxonomy". Many of his writings were in Latin, and his name is rendered in Latin as Carolus Linnæus.

Lifecycle

Complex lifecycle of Anisakis worms Anisakiasis 01.png
Complex lifecycle of Anisakis worms

Anisakis species have complex lifecycles which pass through a number of hosts through the course of their lives. Eggs hatch in seawater, and larvae are eaten by crustaceans, usually euphausids. The infected crustaceans are subsequently eaten by fish or squid, and the nematodes burrow into the wall of the gut and encyst in a protective coat, usually on the outside of the visceral organs, but occasionally in the muscle or beneath the skin. The lifecycle is completed when an infected fish is eaten by a marine mammal, such as a whale, seal, sea lion, dolphin or another animal like a seabird or shark. The nematode excysts in the intestine, feeds, grows, mates, and releases eggs into the seawater in the host's feces. As the gut of a marine mammal is functionally very similar to that of a human, Anisakis species are able to infect humans who eat raw or undercooked fish.

Biological life cycle period involving all different generations of a species succeeding each other through means of reproduction

In biology, a biological life cycle is a series of changes in form that an organism undergoes, returning to the starting state. "The concept is closely related to those of the life history, development and ontogeny, but differs from them in stressing renewal." Transitions of form may involve growth, asexual reproduction, or sexual reproduction.

Larva juvenile form of distinct animals before metamorphosis

A larva is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle.

Krill order of crustaceans

Krill are small crustaceans of the order Euphausiacea, and are found in all the world's oceans. The name "krill" comes from the Norwegian word krill, meaning "small fry of fish", which is also often attributed to species of fish.

The known diversity of the genus has increased greatly since mid-1980s with the advent of modern genetic techniques in species identification. [3] Each final host species was discovered to have its own biochemically and genetically identifiable "sibling species" of Anisakis, which is reproductively isolated. This finding has allowed the proportion of different sibling species in a fish to be used as an indicator of population identity in fish stocks.

Biodiversity Variety and variability of life forms

Biodiversity is the variety and variability of life on Earth. Biodiversity is typically a measure of variation at the genetic, species, and ecosystem level. Terrestrial biodiversity is usually greater near the equator, which is the result of the warm climate and high primary productivity. Biodiversity is not distributed evenly on Earth, and is richest in the tropics. These tropical forest ecosystems cover less than 10 percent of earth's surface, and contain about 90 percent of the world's species. Marine biodiversity is usually highest along coasts in the Western Pacific, where sea surface temperature is highest, and in the mid-latitudinal band in all oceans. There are latitudinal gradients in species diversity. Biodiversity generally tends to cluster in hotspots, and has been increasing through time, but will be likely to slow in the future.

Gene Basic physical and functional unit of heredity

In biology, a gene is a sequence of nucleotides in DNA or RNA that encodes the synthesis of a gene product, either RNA or protein.

Population All the organisms of a given species that live in the specified region

In biology, a population is all the organisms of the same group or species, which live in a particular geographical area, and have the capability of interbreeding. The area of a sexual population is the area where inter-breeding is potentially possible between any pair within the area, and where the probability of interbreeding is greater than the probability of cross-breeding with individuals from other areas.

Morphology

A scanning electron micrograph of the mouthparts of A. simplex So4b-08.jpg
A scanning electron micrograph of the mouthparts of A. simplex

Anisakis share the common features of all nematodes: the vermiform body plan, round in cross section, and a lack of segmentation. The body cavity is reduced to a narrow pseudocoel. The mouth is located anteriorly and surrounded by projections used in feeding and sensation, with the anus slightly offset from the posterior. The squamous epithelium secretes a layered cuticle to protect the body from digestive acids.

Cross section (geometry) the intersection of a body in 3D space with a plane, or the analog in higher-dimensional space. Cutting an object into slices creates many parallel cross sections. A cross section of 3D space that is parallel to two of the axes is a contour line

In geometry and science, a cross section is the non-empty intersection of a solid body in three-dimensional space with a plane, or the analog in higher-dimensional spaces. Cutting an object into slices creates many parallel cross sections. The boundary of a cross section in three-dimensional space that is parallel to two of the axes, that is, parallel to the plane determined by these axes, is sometimes referred to as a contour line; for example, if a plane cuts through mountains of a raised-relief map parallel to the ground, the result is a contour line in two-dimensional space showing points on the surface of the mountains of equal elevation.

Segmentation in biology is the division of some animal and plant body plans into a series of repetitive segments. This article focuses on the segmentation of animal body plans, specifically using the examples of the taxa Arthropoda, Chordata, and Annelida. These three groups form segments by using a "growth zone" to direct and define the segments. While all three have a generally segmented body plan and use a growth zone, they use different mechanisms for generating this patterning. Even within these groups, different organisms have different mechanisms for segmenting the body. Segmentation of the body plan is important for allowing free movement and development of certain body parts. It also allows for regeneration in specific individuals.

Body cavity fluid-filled space in a multicellular organism

A body cavity is any space or compartment, or potential space in the animal body. Cavities accommodate organs and other structures; cavities as potential spaces contain fluid.

As with all parasites with a complex lifecycle involving a number of hosts, details of the morphology vary depending on the host and lifecycle stage. In the stage which infects fish, Anisakis species are found in a distinctive "watch-spring coil" shape. They are roughly 2 cm long when uncoiled. When in the final host, anisakids are longer, thicker, and more sturdy, to deal with the hazardous environment of a mammalian gut.

Health implications

Anisakids pose a risk to human health through intestinal infection with worms from the eating of underprocessed fish, and through allergic reactions to chemicals left by the worms in fish flesh. [4]

Anisakiasis

Anisakiasis
Symptoms of Raw fish infection.png
Differential symptoms of parasite infection by raw fish: Clonorchis sinensis (trematode/fluke), Anisakis (nematode/roundworm) and Diphyllobothrium (cestode/tapeworm), [5] all have gastrointestinal, but otherwise distinct, symptoms. [6] [7] [8] [9]
Specialty Infectious disease

Anisakiasis is a human parasitic infection of the gastrointestinal tract caused by the consumption of raw or undercooked seafood containing larvae of the nematode Anisakis simplex. The first case of human infection by a member of the family Anisakidae was reported in the Netherlands by Van Thiel, who described the presence of a marine nematode in a patient suffering from acute abdominal pain. [10] It is frequently reported in areas of the world where fish is consumed raw, lightly pickled, or salted. The areas of highest prevalence are Scandinavia (from cod livers), Japan (after eating sashimi), the Netherlands (by eating infected fermented herrings (maatjes)), Spain (from eating anchovies and other fish marinated in escabeche ), and along the Pacific coast of South America (from eating ceviche ). The frequency in the United States is unknown, because the disease is not reportable and can go undetected or be mistaken for other illnesses. Anisakiasis was first recognized in the 1960s. During the 1970s, about 10 cases per year were reported in the literature. The frequency is probably much higher, due to home preparation of raw or undercooked fish dishes. In Japan, more than 1,000 cases are reported annually. [11] Development of better diagnostic tools and greater awareness has led to more frequent reporting of anisakiasis.

Within a few hours of ingestion, the parasitic worm tries to burrow though the intestinal wall, but since it cannot penetrate it, it gets stuck and dies. The presence of the parasite triggers an immune response; immune cells surround the worms, forming a ball-like structure that can block the digestive system, causing severe abdominal pain, malnutrition, and vomiting. Occasionally, the larvae are regurgitated. If the larvae pass into the bowel or large intestine, a severe eosinophilic granulomatous response may also occur one to two weeks following infection, causing symptoms mimicking Crohn's disease. [12] [ citation needed ]

Diagnosis can be made by gastroscopic examination, during which the 2-cm larvae are visually observed and removed, or by histopathologic examination of tissue removed at biopsy or during surgery.

Raising consumer and producer awareness about the existence of anisakid worms in fish is a critical and effective prevention strategy. Anisakiasis can be easily prevented by adequate cooking at temperatures greater than 60 °C or freezing. The FDA recommends all shellfish and fish intended for raw consumption be blast frozen to −35 °C or below for 15 hours or be regularly frozen to −20 °C or below for seven days. [11] Salting and marinating will not necessarily kill the parasites, as in Italy where two-third of cases were attributed to anchovies marinated in lemon or vinegar. [13] Humans are thought to be more at risk of anisakiasis from eating wild fish rather than farmed fish. Many countries require all types of fish with potential risk intended for raw consumption to be previously frozen to kill parasites. The mandate to freeze herring in the Netherlands has virtually eliminated human anisakiasis. [14]

Allergic reactions

Even when the fish is thoroughly cooked, Anisakis larvae pose a health risk to humans. Anisakids (and related species such as the sealworm, Pseudoterranova species, and the codworm Hysterothylacium aduncum) release a number of biochemicals into the surrounding tissues when they infect a fish. They are also often consumed whole, accidentally, inside a fillet of fish.

Anisakid larvae in the body cavity of a herring (Clupea harengus) Anisakids.jpg
Anisakid larvae in the body cavity of a herring (Clupea harengus)

Acute allergic manifestations, such as urticaria and anaphylaxis, may occur with or without accompanying gastrointestinal symptoms. The frequency of allergic symptoms in connection with fish ingestion has led to the concept of gastroallergic anisakiasis, an acute IgE-mediated generalized reaction. [10] Occupational allergy, including asthma, conjunctivitis, and contact dermatitis, has been observed in fish processing workers. [15] Sensitivization and allergy are determined by skin-prick test and detection of specific antibodies against Anisakis. Hypersensitivity is indicated by a rapid rise in levels of IgE in the first several days following consumption of infected fish. [10] A 2018 review of cases in France has shown that allergic cases were more commonly found, although the number of human Anisakis infections was decreasing. [16]

Treatment

For the worm, humans are a dead-end host. Anisakis and Pseudoterranova larvae cannot survive in humans, and eventually die. In some cases, the infection resolves with only symptomatic treatment. [17] In other cases, however, infection can lead to small bowel obstruction, which may require surgery, [18] although treatment with albendazole alone (avoiding surgery) has been reported to be successful. Intestinal perforation (an emergency) is also possible. [19]

Occurrence

Larval anisakids are common parasites of marine and anadromous fish (e.g. salmon, sardine), and can also be found in squid and cuttlefish. In contrast, they are absent from fish in waters of low salinity, due to the physiological requirements of krill, which are involved in the completion of the worm's lifecycle. Anisakids are also uncommon in areas where cetaceans are rare, such as the southern North Sea. [20]

Unusual hosts of Anisakis larvae in the Southern hemisphere, rarely reported, include seabirds, sharks, or sea kraits. [21]

Similar parasites

See also

Related Research Articles

<i>Ascaris lumbricoides</i> One of several species of Ascaris

Ascaris lumbricoides is the "large roundworm" of humans, growing to a length of up to 35 cm (14 in). It is one of several species of Ascaris. An ascarid nematode of the phylum Nematoda, it is the most common parasitic worm in humans. This organism is responsible for the disease ascariasis, a type of helminthiasis and one of the group of neglected tropical diseases. An estimated one-sixth of the human population is infected by A. lumbricoides or another roundworm. Ascariasis is prevalent worldwide, especially in tropical and subtropical countries.

Trichinosis Parasitic disease due to invasion by Trichinella spp.

Trichinosis is a parasitic disease caused by roundworms of the Trichinella type. During the initial infection, invasion of the intestines can result in diarrhea, abdominal pain, and vomiting. Migration of larvae to muscle, which occurs about a week after being infected, can cause swelling of the face, inflammation of the whites of the eyes, fever, muscle pains, and a rash. Minor infection may be without symptoms. Complications may include inflammation of heart muscle, central nervous system involvement, and inflammation of the lungs.

Clonorchiasis infectious disease caused by the Chinese liver fluke, Clonorchis sinensis, and two related species

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

<i>Diphyllobothrium</i> genus of worms

Diphyllobothrium is a genus of tapeworms which can cause diphyllobothriasis in humans through consumption of raw or undercooked fish. The principal species causing diphyllobothriasis is Diphyllobothrium latum, known as the broad or fish tapeworm, or broad fish tapeworm. D. latum is a pseudophyllid cestode that infects fish and mammals. D. latum is native to Scandinavia, western Russia, and the Baltics, though it is now also present in North America, especially the Pacific Northwest. In Far East Russia, D. klebanovskii, having Pacific salmon as its second intermediate host, was identified. Other members of the genus Diphyllobothrium include Diphyllobothrium dendriticum, which has a much larger range, D. pacificum, D. cordatum, D. ursi, D. lanceolatum, D. dalliae, and D. yonagoensis, all of which infect humans only infrequently. In Japan, the most common species in human infection is D. nihonkaiense, which was only identified as a separate species from D. latum in 1986. More recently, a molecular study found D. nihonkaiense and D. klebanovskii to be a single species.

Hymenolepiasis is infestation by one of two species of tapeworm: Hymenolepis nana or H. diminuta. Alternative names are dwarf tapeworm infection and rat tapeworm infection. The disease is a type of helminthiasis which is classified as a neglected tropical disease.

Gnathostomiasis is the human infection caused by the nematode (roundworm) Gnathostoma spinigerum and/or Gnathostoma hispidum, which infects vertebrates.

<i>Trichinella spiralis</i> species of worm

Trichinella spiralis is an viviparous nematode parasite, occurring in rodents, pigs, bears, hyenas and humans, and is responsible for the disease trichinosis. It is sometimes referred to as the "pork worm" due to it being typically encountered in undercooked pork products. It should not be confused with the distantly related pork tapeworm.

<i>Echinostoma</i> genus of worms

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

Eucestoda is the larger of the two subclasses of flatworms in the class Cestoda. The Eucestoda are commonly referred to as tapeworms. Larvae have six posterior hooks on the scolex (head), in contrast to the ten-hooked Cestodaria. All tapeworms are endoparasites of vertebrates, living in the digestive tract or related ducts. Examples are the pork tapeworm with a human definitive host, and pigs as the secondary host, and Moniezia expansa, the definitive hosts of which are ruminants.

Gnathostoma spinigerum is a parasitic nematode that causes gnathostomiasis in humans, also known as its clinical manifestations are creeping eruption, larva migrans, Yangtze edema, Choko-Fuschu Tua chid and wandering swelling. Gnathostomiasis in animals can be serious, and even fatal. The first described case of gnathostomiasis was in a young tiger that died in the London Zoo in 1835. The larval nematode is acquired by eating raw or undercooked fish and meat.

<i>Dioctophyme renale</i> species of worm

Dioctophyme renale, commonly referred to as the giant kidney worm is a parasitic roundworm whose mature form is found in the kidneys of mammals. D. renale is distributed worldwide, but is less common in Africa and Oceania. It affects fish eating mammals, particularly mink and dogs. Human infestation is rare, but results in kidney destruction, usually of one kidney and hence not fatal. A 2019 review listed a total of 37 known human cases of dioctophymiasis in 10 countries with the highest number (22) in China. Upon diagnosis through tissue sampling, the only treatment is surgical excision.

Capillaria philippinensis is a parasitic nematode which causes intestinal capillariasis. This sometimes fatal disease was first discovered in Northern Luzon, Philippines in 1964. Cases have also been reported from China, Egypt, Indonesia, Iran, Japan, Korea, Lao PDR, Taiwan and Thailand. Cases diagnosed in Italy and Spain were believed to be acquired abroad, with one case possibly contracted in Colombia. The natural life cycle of C. philippinensis is believed to involve fish as intermediate hosts, and fish-eating birds as definitive hosts. Humans acquire C. philippinensis by eating small species of infested fish whole and raw.

Anisakidae family of worms

The Anisakidae are a family of intestinal nematodes (roundworms). The larvae of these worms can cause anisakiasis when ingested by humans, in raw or insufficiently cooked fish.

Fish disease and parasites disease that afflicts fish

Like humans and other animals, fish suffer from diseases and parasites. Fish defences against disease are specific and non-specific. Non-specific defences include skin and scales, as well as the mucus layer secreted by the epidermis that traps microorganisms and inhibits their growth. If pathogens breach these defences, fish can develop inflammatory responses that increase the flow of blood to infected areas and deliver white blood cells that attempt to destroy the pathogens.

Gnathostoma hispidum is a nematode (roundworm) that infects many vertebrate animals including humans. Infection of Gnathostoma hispidum, like many species of Gnathostoma causes the disease gnathostomiasis due to the migration of immature worms in the tissues.

Eustrongylidosis is a parasitic disease that mainly affects wading birds worldwide; however, the parasite’s complex, indirect life cycle involves other species such as aquatic worms and fish. Moreover, this disease is zoonotic which means the parasite can transmit disease from animals to humans. Eustrongylidosis is named after the causative agent Eustrongylides and typically occurs in eutrophicated waters where concentrations of nutrients and minerals are high enough to provide ideal conditions for the parasite to thrive and persist. Because eutrophication has become a common issue due to agricultural runoff and urban development, cases of Eustrongylidosis are becoming prevalent and hard to control. Eustrongylidosis can be diagnosed before or after death by observing behavior, clinical signs and performing fecal flotations and necropsies. Methods to control Eustrongylidosis include preventing eutrophication and providing hosts with uninfected food sources in aquaculture farms. Parasites are known to be indicators of environmental health and stability and should therefore be studied further to better understand the parasite’s life cycle and how it affects predator-prey interactions and improve conservation efforts.

<i>Anisakis simplex</i> species of worm

Anisakis simplex, known as the herring worm, is a species of nematodes in the genus Anisakis, which occurs in ocean fish such as herrings. Human infections can cause severe abdominal cramps. The worm drills through the intestinal wall and lodges in muscle tissue.

<i>Contracaecum</i> genus of worms

Contracaecum is genus of parasitic nematodes from the family Anisakidae. These nematodes are parasites of warm-blooded, fish eating animals, i.e. mammals and birds, as sexually mature adults. The eggs and the successive stages of their larvae use invertebrates and increasing size classes of fishes as intermediate hosts. It is the only genus in the family Anisakidae which can infect terrestrial, marine and freshwater animals.

References

  1. Berger SA, Marr JS (2006). Human Parasitic Diseases Sourcebook. Jones and Bartlett Publishers: Sudbury, Massachusetts
  2. Dujardin F. (1845). Histoire naturelle des helminthes ou vers intestinaux. xvi, 654+15 pp. (Anisakis: p. 220) Open Access logo PLoS transparent.svg
  3. Mattiucci, S.; Nascetti, G. (15 June 2006). "Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update". Parasite. 13 (2): 99–113. doi:10.1051/parasite/2006132099. PMID   16800118.
  4. Amato Neto V, Amato JG, Amato VS (2007). "Probable recognition of human anisakiasis in Brazil". Rev. Inst. Med. Trop. Sao Paulo. 49 (4): 261–62. doi:10.1590/s0036-46652007000400013. PMID   17823758.
  5. WaiSays: "About Consuming Raw Fish" Retrieved on April 14, 2009
  6. For Chlonorchiasis: Public Health Agency of Canada > Clonorchis sinensis – Material Safety Data Sheets (MSDS) Retrieved on April 14, 2009
  7. For Anisakiasis: WrongDiagnosis: "Symptoms of Anisakiasis" Retrieved on April 14, 2009
  8. For Diphyllobothrium: MedlinePlus > "Diphyllobothriasis" Updated by: Arnold L. Lentnek, MD. Retrieved on April 14, 2009
  9. For symptoms of diphyllobothrium due to vitamin B12-deficiency University of Maryland Medical Center > "Megaloblastic (Pernicious) Anemia" Retrieved on April 14, 2009
  10. 1 2 3 Audicana, Maria Teresa; Kennedy, MW (2008). "Anisakis Simplex: From Obscure Infectious Worm to Inducer of Immune Hypersensitivity". Clinical Microbiology Reviews. 21 (2): 360–79. doi:10.1128/CMR.00012-07. PMC   2292572 . PMID   18400801.
  11. 1 2 Bad Bug Book: Foodborne Pathogens Microorganisms and Natural Toxins Handbook, 2nd edition Food and Drug Administration.
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  13. Guardone, Lisa; Armani, Andrea; Nucera, Daniele; Costanzo, Francesco; Mattiucci, Simonetta; Bruschi, Fabrizio (30 July 2018). "Human anisakiasis in Italy: a retrospective epidemiological study over two decades". Parasite. 25: 41. doi:10.1051/parasite/2018034. PMC   6065268 . PMID   30058531.
  14. John, David T.; William Petri (2006). Markell and Voge's Medical Parasitology. St. Louis: Saunders. pp. 267–70. ISBN   978-0-7216-7634-0.
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  16. Yera, Hélène; Fréalle, Émilie; Dutoit, Emmanuel; Dupouy-Camet, Jean (11 April 2018). "A national retrospective survey of anisakidosis in France (2010-2014): decreasing incidence, female predominance, and emerging allergic potential". Parasite. 25: 23. doi:10.1051/parasite/2018016. PMC   5894341 . PMID   29637891.
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  19. Pacios, Enrique; Arias-Diaz, Javier; Zuloaga, Jaime; Gonzalez-Armengol, Juan; Villarroel, Pedro; Balibrea, Jose L. (December 2005). "Albendazole for the Treatment of Anisakiasis Ileus". Clinical Infectious Diseases. 41 (12): 1825–1826. doi:10.1086/498309. PMID   16288416.
  20. Grabda, Jadwiga (30 June 1976). "Studies on the life cycle and morphogenesis of Anisakis simplex (Rudolphi, 1809) (Nematoda: Anisakidae) cultured in vitro". Acta Ichthyologica et Piscatoria. 06 (1): 119–141. doi:10.3750/AIP1976.06.1.08.
  21. Shamsi, Shokoofeh; Briand, Marine J.; Justine, Jean-Lou (December 2017). "Occurrence of Anisakis (Nematoda: Anisakidae) larvae in unusual hosts in Southern hemisphere". Parasitology International. 66 (6): 837–840. doi:10.1016/j.parint.2017.08.002. PMID   28797592.
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