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      Anisakis Nematodes in Fish and Shellfish- from infection to allergies

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          Abstract

          Anisakidosis is a zoonotic parasitosis induced by members of the family Anisakidae. The anisakid genera includes Anisakis, Pseudoterranova, Hysterothylacium and Contracaecum. The final definitive hosts of these nematodes are marine mammals with a complex life cycle. These nematode parasites use different crustaceans and fish species as intermediate or paratenic hosts and humans are accidental hosts. Human anisakiasis, the infections caused by members of the genus Anisakis, occurs , when seafoods, particularly fish, contaminated with the infective stage (third stage larvae [L3]) of this parasite, are consumed. Pseudoterranovosis, on the other hand is induced by members of the genus Pseudoterranova. These two genera of anisakids have been implicated in human disease globally. There is a rise in reports of gastro-intestinal infections accompanied by allergic reactions caused by Anisakis simplex and Anisakis pegreffii. This review provides an update on current knowledge on Anisakis as a food-borne parasite with special focus on the increasingly reported diversity of fish and crustacean hosts, allergens and immunological cross-reactivity with invertebrate proteins rendering this parasite a significant public health issue.

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          Highlights

          • Anisakis, is a foodborne zoonotic parasite.

          • Humans are accidental hosts of Anisakis L3 larva.

          • Consumption of Anisakis parasite-contaminated seafood causes human anisakiasis.

          • Zooplankton (Crustaceans: Krills, Squids, Crayfish) composition in fishing regions contribute to Anisakis parasitosis.

          • Anisakis is the parasite with the largest number of registered allergens with the IUIS.

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          Most cited references137

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          Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity.

          Infection of humans with the nematode worm parasite Anisakis simplex was first described in the 1960s in association with the consumption of raw or undercooked fish. During the 1990s it was realized that even the ingestion of dead worms in food fish can cause severe hypersensitivity reactions, that these may be more prevalent than infection itself, and that this outcome could be associated with food preparations previously considered safe. Not only may allergic symptoms arise from infection by the parasites ("gastroallergic anisakiasis"), but true anaphylactic reactions can also occur following exposure to allergens from dead worms by food-borne, airborne, or skin contact routes. This review discusses A. simplex pathogenesis in humans, covering immune hypersensitivity reactions both in the context of a living infection and in terms of exposure to its allergens by other routes. Over the last 20 years, several studies have concentrated on A. simplex antigen characterization and innate as well as adaptive immune response to this parasite. Molecular characterization of Anisakis allergens and isolation of their encoding cDNAs is now an active field of research that should provide improved diagnostic tools in addition to tools with which to enhance our understanding of pathogenesis and controversial aspects of A. simplex allergy. We also discuss the potential relevance of parasite products such as allergens, proteinases, and proteinase inhibitors and the activation of basophils, eosinophils, and mast cells in the induction of A. simplex-related immune hypersensitivity states induced by exposure to the parasite, dead or alive.
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            Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes.

            The application of molecular systematics to the anisakid nematodes of the genera Anisakis, Pseudoterranova and Contracaecum, parasites of aquatic organisms, over the last two decades, has advanced the understanding of their systematics, taxonomy, ecology and phylogeny substantially. Here the results of this effort on this group of species from the early genetic works to the current status of their revised taxonomy, ecology and evolutionary aspects are reviewed for each of three parasitic groups. It has been shown that many anisakid morphospecies of Anisakis, Contracaecum and Pseudoterranova include a certain number of sibling species. Molecular genetic markers provided a rapid, precise means to screen and identify several species that serve as definitive and intermediate and or/paratenic hosts of the so far genetically characterized species. Patterns of differential distribution of anisakid nematodes in various definitive and intermediate hosts are presented. Differences in the life history of related species can be due both to differential host-parasite co-adaptation and co-evolution, and/or to interspecific competition, that can reduce the range of potential hosts in sympatric conditions. Phylogenetic hypotheses attempted for anisakid nematodes and the possible evolutionary scenarios that have been proposed inferred from molecular data, also with respect to the phylogeny of their hosts are presented for the parasite-host associations Anisakis-cetaceans and Contracaecum-pinnipeds, showing that codivergence and host-switching events could have accompanied the evolution of these groups of parasites. Finally, examples in which anisakid nematodes recognized genetically at the species level in definitive and intermediate/paratenic hosts from various geographical areas of the Boreal and Austral regions and their infection levels have been used as biological indicators of fish stocks and food-web integrity in areas at high versus low levels of habitat disturbance (pollution, overfishing, by-catch) are presented.
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              Molecular Epidemiology of Anisakis and Anisakiasis: An Ecological and Evolutionary Road Map.

              This review addresses the biodiversity, biology, distribution, ecology, epidemiology, and consumer health significance of the so far known species of Anisakis, both in their natural hosts and in human accidental host populations, worldwide. These key aspects of the Anisakis species' biology are highlighted, since we consider them as main driving forces behind which most of the research in this field has been carried out over the past decade. From a public health perspective, the human disease caused by Anisakis species (anisakiasis) appears to be considerably underreported and underestimated in many countries or regions around the globe. Indeed, when considering the importance of marine fish species as part of the everyday diet in many coastal communities around the globe, there still exist significant knowledge gaps as to local epidemiological and ecological drivers of the transmission of Anisakis spp. to humans. We further identify some key knowledge gaps related to Anisakis species epidemiology in both natural and accidental hosts, to be filled in light of new 'omic' technologies yet to be fully developed. Moreover, we suggest that future Anisakis research takes a 'holistic' approach by integrating genetic, ecological, immunobiological, and environmental factors, thus allowing proper assessment of the epidemiology of Anisakis spp. in their natural hosts, in human populations, and in the marine ecosystem, in both space and time.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                06 June 2019
                August 2019
                06 June 2019
                : 9
                : 384-393
                Affiliations
                [a ]School of Science, Discipline of Biosciences and Food Technology, Royal Melbourne Institute of Technology (RMIT) University, Bundoora, Victoria, Australia
                [b ]Molecular Allergy Research Laboratory, Department of Molecular and Cell Biology, James Cook University, Townsville, Queensland, Australia
                [c ]Australian Institute of Tropical Health and Medicine, James Cook University, Townsville, Queensland, Australia
                [d ]College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Queensland, Australia
                Author notes
                []Corresponding author. College of Public Health, Medical and Veterinary Sciences Room 109A, DB47, Pharmacy and Medical Research, James Cook University, Angus Smith Drive, Douglas, QLD, 4811, Australia. andreas.lopata@ 123456jcu.edu.au
                Article
                S2213-2244(19)30002-1
                10.1016/j.ijppaw.2019.04.007
                6626974
                31338296
                5d9c2770-76d8-4cbb-a607-e9ef3458e418
                © 2019 Published by Elsevier Ltd on behalf of Australian Society for Parasitology.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 4 February 2019
                : 19 April 2019
                : 20 April 2019
                Categories
                Special section: Emerging Zoonoses and Wildlife

                anisakis,fish hosts,crustacean hosts,shellfish,anisakiasis,anisakis allergy,cross-reactivity,zoonotic,food-borne parasite

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