Foodborne anisakiasis and allergy

doi:10.1016/j.mcp.2014.02.003

Molecular and Cellular Probes

Volume 28, Issue 4, August 2014, Pages 167-174

https://doi.org/10.1016/j.mcp.2014.02.003 Get rights and content

Abstract

Human anisakiasis, a disease caused by Anisakis spp. (Nematoda), is often associated with clinical signs that are similar to those associated with bacterial or viral gastroenteritis. With the globalisation of the seafood industry, the risk of humans acquiring anisakiasis in developed countries appears to be underestimated. The importance of this disease is not only in its initial manifestation, which can often become chronic if the immune response does not eliminate the worm, but, importantly, in its subsequent sensitisation of the human patient. This sensitisation to Anisakis-derived allergens can put the patient at risk of an allergic exacerbation upon secondary exposure. This article reviews some aspects of this food-borne disease and explains its link to chronic, allergic conditions in humans.

Introduction

Gastrointestinal worms represent a huge global burden of disease, with more than 2.5 billion people infected [1]. These worms are usually contracted through the ingestion of infective eggs or larvae, or through larval penetration of the skin [2]. Traditionally, these parasites are much more prevalent in developing than developed countries [3]. Some nematodes, such as Necator americanus (hookworm) and Trichuris trichiura (whipworm), are actually thought to be beneficial in preventing the development of allergy and other chronic inflammatory conditions, such as colitis, through their anti-inflammatory or immuno-modulatory excretory/secretory (ES) molecules [4], [5], [6]. In contrast, other nematodes, such as Anisakis simplex sensu stricto (s.s.), are the causes of such allergic diseases [7], [8].

Anisakid nematodes (Nematoda: Anisakidae) affect a growing number of people in developed countries. Commonly reported species are Anisakis simplex (s.s.) and Anisakis pegreffii, and are known as herring, seal or cod worms. They were first implicated as a cause of gastrointestinal illness in 1876 [9], with immunological confirmation in the early 1980s [10], [11]. The causative agent was later described by van Thiel et al. [12] in a Dutch patient, who had consumed raw herring. Since this discovery, more than 20,000 cases have been reported worldwide, with the majority of cases being in Japan, where, today, 2000–3000 cases are reported annually [13], [14]. Anisakidosis refers to the disease caused by any member of the family Anisakidae, whereas anisakiasis is caused by members of the genus Anisakis. This brief review focuses on anisakiasis and its significance in relation to chronic, allergic conditions.

Section snippets

Anisakid biology

Different anisakids can be found in different cetacean hosts, depending on local environments [2], [15], [16]. Genetically confirmed A. simplex (s.s.) has been recorded in nine species of cetacean hosts, whereas A. pegreffii has been found as an adult in three species of dolphin (family Delphinidae) [17]. Infected cetacean definitive hosts excrete Anisakis eggs in their faeces into the aquatic environment. Individual first-(L1) and then second-stage (L2) larvae develop inside these eggs.

Molecular identification and classification of anisakids

There are many species of Anisakis which can vary considerably in their host and geographical distributions as well as biology (reviewed in Ref. [17]). For example, it has been reported that A. simplex (s.s.) penetrates the musculature of Scomber japonicas (mackerel) better than A. pegreffii, leading to increased establishment and a higher intensity of infection [26]. Anisakis represents a complex of species [16], and is related to species of Pseudoterranova and Contracaecum based on the

Geographical and host distributions

The Anisakis species within Clade I are distributed mainly in the Atlantic Ocean, and the East and West Pacific, where their definitive hosts (family Delphinidae) are common. The distribution of A. simplex (s.s.) and A. pegreffii extends throughout the Mediterranean sea, with both species reaching as far north as the Arctic Circle and as far south as the Antarctic waters [43]. Multiple anisakid species can be isolated from one parasitised fish. For example, Scomber japonicus (chub mackerel)

Prevalence in humans

Ingestion of anisakid larvae typically leads to a self-limiting infection, which sensitises the human host to Anisakis allergens (cf. Section 7). The country with the highest prevalence of Anisakis infections in humans is Japan. Infected sushi and sashimi (national dishes of raw fish) are a significant source of human infection, with 2000–3000 cases of anisakiasis being reported annually [14]. The globalisation of provincial cuisine has also increased the number and distribution of consumers

Allergic responses in humans and anisakid allergens

Although some helminths do not usually induce allergic responses in humans, anisakids often do. Clinical signs include urticaria, rhinitis, bronco-constriction, cough and/or gastrointestinal responses [2], [20]. Frequently, acute allergic reactions can be seen, with no or minor gastrointestinal problems. On the other hand, gastrointestinal symptoms sometimes occur without an allergic component. In relation to anisakids, the predominant response seems to be Th2-mediated, resulting in the

Food safety considerations

The consumption of food and food products has altered considerably over the last few centuries due to the development of new modes of transport, agriculture, population growth and globalisation. The World Health Organization (WHO) states that the total consumption of fish has been increasing at a rate of 3.6% per year since 1961 [99]. The average apparent consumption per capita increased from approximately 9 kg in the early 1960s to 16 kg in 1997, showing that demand has nearly doubled in 40

Conclusion

A. simplex and A. pegreffii are well known parasitic pathogens of humans in countries such as Japan, where the provincial cuisine includes raw or undercooked fish. In the last few years, these nematodes have been newly discovered in Chinese and Australian waters, where local fish species act as paratenic hosts. Recently, sea lamprey has been described as a new paratenic host, which could account for the spread of Anisakis larvae into both fresh and sea waters [18]. The increased number of new

Acknowledgements

Financial support from the Australian Research Council (ARC) to AL is acknowledged. AL is holder of an ARC Future Fellowship. Financial support from a JCU Centre of Biodiscovery & Molecular Development of Therapeutics Seed Grant to FB and the ABRS to AL and RG is acknowledged. The Gasser Lab is supported by grants from the ARC and the National Health and Medical Research Council (NHMRC).

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Cited by (90)

A novel rhabdovirus detected in Anisakis larvae distributed in the coastal areas of Japan: Viral genome analysis and possible coevolutionary relationship between virus and host nematodes
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In the last decade, it has become evident that various RNA viruses infect helminths including Order Ascaridida. However, there is still no information available for viruses infecting Anisakis. We herewith demonstrate the presence of a novel rhabdovirus from Anisakis larvae detected by next-generation sequencing analysis and following RT-PCR. We determined the nearly all nucleotide sequence (12,376 nucleotides) of the viral genome composed of seven open reading frames, and we designated the virus as Suzukana rhabdo-like virus (SkRV). BLASTx search indicated that SkRV is a novel virus belonging to the subfamily Betanemrhavirus, rhabdovirus infecting parasitic nematodes of the Order Ascaridida. SkRV sequence was detectable only in the total RNA but not in the genomic DNA of Anisakis, ruling out the possibility of SkRV being an endogenous viral element incorporated into the host genomic DNA. When we individually tested Anisakis larvae obtained from Scomber japonicus migrating in the coastal waters of Japan, not all but around 40% were SkRV-positive. In the phylogenetic trees of Betanemrhavirus and of the host Ascaridida nematodes, we observed that evolutional distances of viruses were, to some extent, parallel with that of host nematodes, suggesting that viral evolution could have been correlated with evolution of the host. Although biological significance of SkRV on Anisakis larvae is still remained unknown, it is interesting if SkRV were somehow related to the pathogenesis of anisakiasis, because it is important matter of public health in Japan and European countries consuming raw marine fishes.
The involvement of Pseudoterranova decipiens fish infestation on the shelf-life of fresh Atlantic cod (Gadus morhua) fillet
2024, International Journal of Food Microbiology
Zoonotic nematodes of the family Anisakidae are highly common in many marine fish species, which act as paratenic hosts for the third larval stage. In the fish, these parasites may migrate from the fish's gastro-intestinal tract (GI-tract) further to the coelomic cavity and muscles, making them a possible contamination source of bacteria they carry on their cuticle and in their GI-tract. A previous study revealed no apparent effect of Anisakis simplex on spoilage of fish, but the equally common anisakid species Pseudoterranova decipiens has a larger body surface potentially increasing the bacterial load brought into the fish muscle upon migration. As the presence of shelf-life reducing spoilage bacteria in the microbiome of this anisakid species has been demonstrated, the objective of the present study was to assess the potential shelf-life reducing effect of P. decipiens in fresh fish fillets stored in a domestic refrigerator.
Atlantic cod was used as a model since members of the cod family are the third most consumed marine fish globally and it has the highest prevalence of P. decipiens infections. Infected and non-infected codfish fillet portions were collected and microbiologically analyzed at day 0 and day 4 of storage in a domestic fridge. Three isolation media were used to enhance maximum bacterial recovery and isolates were identified using MALDI-TOF MS and 16S rRNA gene sequencing. In parallel to the microbiological examination, sensory analysis was performed daily on the cod fillets to evaluate the freshness of the fish.
Results revealed the presence of typical spoilage bacteria (e.g., Pseudomonas sp., Photobacterium sp.) in all fish, but based on the total viable counts, total H₂S-producing bacteria, and sensory analysis, there were no objective indications to assume an increased fish spoilage rate by the presence and migration P. decipiens. Additionally, a beta-diversity comparison revealed no significant differences in microbiota composition between infected and non-infected fish parts, though individual heterogeneity in microbiome composition among Atlantic codfish individuals was found. As total viable counts did, however, exceed the guideline limits for fresh fish, further research should now focus on the role of the candling step as a potential source of post-harvest contamination. As such, anisakid infection might still accelerate fish spoilage, though now in an indirect way.
Unraveling the microbiota of the fish parasite Pseudoterranova decipiens in codfish (Gadus morhua) reveals a fish-related bacterial community
2022, International Journal of Food Microbiology
Citation Excerpt :
This nematode family, mainly represented by species of the genera Anisakis, Pseudoterranova and Contracaecum, usually migrates from the fish's gastro-intestinal tract (GI-tract) to the coelomic cavity where they remain attached to internal organs. The larvae also have the ability to migrate further to the fish muscles which poses an important problem to the fish industry (Baird et al., 2014). Specifically, their presence reduces the marketability and commercial value due to the negative perception of consumers with an estimated loss of $26–$50 million per year for some fish species (Bao et al., 2018).
Anisakidae, mainly represented by the species Anisakis simplex and Pseudoterranova decipiens, are one of the most commonly zoonotic nematodes present in marine fish species. Apart from public health risks directly linked to the parasite itself, little is known on the effects of the migrating nematodes on the hygienic quality of the fish fillet due to bacteria it carries. In the present study, the cultivated bacterial community on and in individual P. decipiens larvae deriving from codfish is reported. Four isolation media were included and evaluated to increase the bacterial diversity isolated, and identification of the bacterial growth was performed by a combination of Matrix-Assisted Laser Desorption Ionization Time-Of-Flight mass spectrometry and 16S rRNA gene sequencing. Results revealed that the microbiota of P. decipiens larvae comprises both potential spoilage bacteria and human opportunistic pathogens, and that a combined isolation on the general isolation medium tryptone soy agar and a medium supplemented with artificial seawater resulted in the highest bacterial recovery in terms of diversity and enumeration. Dissimilarity analysis also revealed similar, though unique, bacterial communities between nematodes originating from the same fish suggesting that anisakid microbiota compositions are reflections of the microbial assemblages in the fish host as an individual, and that the gut microbiome is diverse within gadoid fish species originating from the same geographical habitat. Future research should, based on the results in the present study, further elaborate on the comparison of the bacterial communities of both the larva and the codfish from which it was isolated, and, explore the extrapolation potential towards other fish and nematode species. Also, the actual degree of risk beyond the simple presence of the parasite due to carriage of opportunistic bacteria should be examined, as well as the nematode's true effect on spoilage.
Anisakis notification in fish: An assessment of the cases reported in the European Union rapid alert system for food and feed (RASFF) database
2021, Food Control
The presence of Anisakis spp. in fishery products are of enormous relevance to consumers, food security authorities and the fishing and food industries, because of the associated disease and possible loss of commercial value. Moreover, due to the great increase in the consumption of raw or undercooked fish, this study evaluated the notification of Anisakis reported on the RASFF portal from 1979 to 2019. The results show that although the first notification to Anisakis appeared in 2001, the highest number of cases occurred between 2011 and 2019. The 546 notifications to Anisakis were carried out by 13 different European Union countries. Italy, in addition to report the largest number of cases, was the only country to report every year. The higher notifications cases are for Spanish products. The main notified fish were: Mackerel, Hake and Anglerfish. The main type of notification was “border rejection” (25.28%), followed by “alert” (23.81%). Most of the “notification bases”, consisted of “official control on the market” (56.78%). The main measures taken for Anisakis' notifications were “destruction” (27.5%) and “withdrawal from the market” (17.8%). As for the distribution status, it was observed that the majority was “no distribution” (22.71%) or “distribution on the market possible” (21.06%). Regarding the risk decision, the vast majority of cases were considered “undecided”. Despite presenting some gaps, the RASFF portal represents a useful tool in obtaining information on trends in notification of Anisakis occurring in fish. The significant increase in notifications to Anisakis in recent years, reinforces the need for a standardization of the methodologies for detecting parasites, using more modern techniques. Consumers play an important role in the fishing chain, and it is necessary to promote continuing education, so that citizens can become an active part in the management of the risks related to fish intake associated with Anisakis larvae.
Expression and functionality of allergenic genes regulated by simulated gastric juice in Anisakis pegreffii
2021, Parasitology International
Citation Excerpt :
Previous studies only generated lists of putative parasite allergens based on comparative analyses of next-generation sequencing (NGS) and bioinformatics. To date, a total of 14 A. simplex allergens have been identified [13,14]. Most Anisakis allergens have been detected in the excretory/secretory (ES) products of the parasite, such as Ani s 1, Ani s 7, and Ani s 9 [15,16].
To better understand the molecular mechanisms underlying allergens and parasite immunity and discover the stage-enriched gene expression of fish-borne zoonotic nematodes in the stomach, we used RNA-seq to study the transcriptome profiles of Anisakis pegreffii (Nematoda: Anisakidae, AP) in simulated gastric juice. Mobile L3 larvae were incubated in simulated medium at 37 °C in 5% CO₂ (AP-GJ) and the control group larvae were collected in PBS under the same conditions (AP-PBS). We found that the sequences of A. pegreffii were highly similar to Toxocara canis sequences. Among the transcripts, there would be 138 up-regulated putative genes and 251 down-regulated putative genes in AP-GJ group. Several lipid binging-related genes were more highly expressed in AP-GJ larvae. Moreover, 17 allergen genes were up-regulated and 29 were down-regulated in AP-GJ larvae. Eleven allergen genes belonged to one or more of the following three categories: biological process, cellular component, and molecular function. According to KEGG analysis, the main pathways that were represented included protein processing in transcription, immune system, cancer, and infectious disease. In particular, the most significant changes in the expression of parasite-derived allergen products occurred in AP-GJ larvae. This study helps us to extend our understanding of the biology of the fish-borne zoonotic parasite A. pegreffii and could be helpful for more precise risk assessment and providing guidelines for allergic consumers.
Multidisciplinary approach in study of the zoonotic Anisakis larval infection in the blue mackerel (Scomber australasicus) and the largehead hairtail (Trichiurus lepturus) in Northern Taiwan
2020, Journal of Microbiology, Immunology and Infection
Citation Excerpt :
The life cycles of Anisakis utilized the aquatic ecosystem, involves various hosts at different levels of the food web. Many teleosts and cephalopods act as intermediate or paratenic hosts of the Anisakis nematodes.2–4 The cycle is accomplished upon infected fish or squid eaten by a marine mammal.5
Anisakid larvae are the food-borne pathogen highly prevalent among numerous marine fishes. Accidental consumption of infected raw or poorly cooked fish fillets may cause anisakiasis.
This study used the multidisciplinary approach to investigate the occurrence of Anisakis nematodes in commonly consumed fish species, Scomber australasicus and Trichiurus lepturus purchased in Taipei Xinyi traditional fish market.
All the Anisakis larvae collected herein were identified morphologically as Anisakis type I or Anisakis type II. The prevalence and the mean intensity of Anisakis larvae collected from S. australasicus was 80.77%, 26.8 (10–32) and 100%, 49.0 (27–70) for T. lepturus. Using molecular analysis, 83.33% (180/216) were identified as Anisakis pegreffii, 6.05% (13/216) as Ascaris typica, 1.85% (4/216) as Ascaris physeteris and 8.80% (19/216) as hybrid genotype (A. pegreffii + Anisakis simplex) in S. australasicus. In T. lepturus, 86.31% (290/336) were identified as A. pegreffii, 2.38% (8/336) as A. typica, and 11.31% (38/336) as hybrid genotype (A. pegreffii + A. simplex [s.s]). The molecular phylogenetic analysis shows two cluster clades, one group includes A. pegreffii complex and the other include Ascaris paggiae, Ascaris brevispiculata, and A. physeteris.
Thus, A. pegreffii is the most abundant species and may be the potential causes of human infection.

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Foodborne anisakiasis and allergy

Abstract

Introduction

Section snippets

Anisakid biology

Molecular identification and classification of anisakids

Geographical and host distributions

Prevalence in humans

Allergic responses in humans and anisakid allergens

Food safety considerations

Conclusion

Acknowledgements

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Int J Parasitol

Int J Parasitol

Food Control

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Int J Food Microbiol

Parasitol Int

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Int J Food Microbiol

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Int J Parasitol

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Polar Sci

Mol Cell Probes

Parasitol Int

J Allergy Clin Immunol

Trends Parasitol

J Allergy Clin Immunol

Parasitol Int

Parasitol Int

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Int J Parasitol

Mol Biochem Parasitol

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Mol Biochem Parasitol

Trends Parasitol

Trends Parasitol

Hum Immunol

J Immunol Methods

Comput Biol Chem

Soil-transmitted helminths

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

Clin Microbiol Rev

Hookworm excretory/secretory products induce IL-4+IL-10+ CD4+ T cell responses and suppress pathology in a mouse model of colitis

Infect Immun

Review article: helminths as therapeutic agents for inflammatory bowel disease

Aliment Pharmacol Ther

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J Gastroenterol Hepatol

New insights into seafood allergy

Curr Opin Allergy Clin Immunol

Die menschlichen Parasiten und die von ihren herruehrenden Krankheiten

Studies on the etiologic mechanism of anisakiasis. –1. Immunological reactions of digestive tract induced by Anisakis larva

Gastroenterol Jpn

Detection of Anisakis larvae crude antigen specific IgE by means of enzyme linked immunosorbent assay

Arerugi

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Anisakidosis: perils of the deep

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Endoscopic findings and clinical manifestation of gastric anisakiasis

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