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ALLERGIES IN THE WORKPLACE
ALLSA RESEARCH AWARDS REPORT
APPROACHES TO DIAGNOSING ANISAKIS
The management of anisakiasis involves physically removing the larvae, if possible, or treating the patientwith antihelminthics, anti-inflammatories and anal- Natalie Nieuwenhuizen,1 BSc(Med) Hons, PhD
gesics.3,4 The Anisakis larvae cannot survive or repro-duce in humans, but if the larvae are not removed, the Mohamed Jeebhay,2 MBChB, DOH, MPhil (Epi),
disease can become chronic as inflammatory cells sur- round the larval remains and lead to symptoms which Andreas L Lopata,1,3 MSc, PhD (Med Science)
can mimic dyspepsia, Crohn’s syndrome, appendicitis, 1Division of Immunology, Institute of Infectious irritable bowel syndrome, diverticulitis, non-specific Diseases and Molecular Medicine, Faculty of Health eosinophilic enteritis, or even gastric cancer.2 Science, University of Cape Town, South Africa Abdominal pain, nausea, vomiting and/or diarrhoea 2Centre for Occupational and Environmental Health within 48 hours of consuming fresh seafood should Research, School of Public Health and Family indicate the possibility of Anisakis infection. As many Medicine, University of Cape Town, South Africa cases of anisakiasis have occurred after consumptionof freshly caught fish that appeared well-cooked but 3Allergy Research Group, School of Applied Science, was not sufficiently heated through to kill larvae, inges- Royal Melbourne Institute of Technology, Bundoora tion of raw seafood should not be the only factor mer- iting further investigation. In order to kill larvae, fishshould be frozen at –20°C for at least 24 hours orcooked so that all parts of the fish reach at least 60°Cfor 10-20 minutes.2 Smoking fish or marinating it in lemon juice or vinegar does not kill Anisakis.
Anisakis is a parasitic nematode which infects fishand can cause gastrointestinal disease if accidental- ANISAKIS ALLERGY
ly ingested. Infection can be accompanied by severe Of particular relevance to the physician is that Anisakis allergic reactions such as urticaria, angio-oedema can also cause severe allergic reactions because of its and anaphylaxis. Furthermore, workers involved in ability to elicit strong Th2 responses.5,6 Many patients fish processing can develop occupational allergy to experience gastroallergic anisakiasis, in which infection Anisakis, including asthma, rhinoconjunctivitis andprotein contact dermatitis. Diagnosis of allergy toAnisakis relies on skin-prick tests and the detectionof specific IgE by ImmunoCAP. Since Anisakisinfests fish, fish allergy should be investigated insymptomatic patients. Anisakis proteins alsodemonstrate considerable immunological cross-reactivity to proteins of related nematodes and otherinvertebrates such as house-dust mites and cock-roaches; this needs to be borne in mind when thediagnosis is made. This review outlines theapproaches that have been used to increase thespecificity of Anisakis diagnosis, including the use ofimmunoblotting and the identification of Anisakisallergens.
ANISAKIS INFECTION
Anisakis species are marine roundworms which use
sea mammals such as dolphins and whales as primary
hosts. The stage 3 larval form (L3) of Anisakis (Fig. 1)
infects fish and other seafood such as squid, and con-
sequently humans may become accidental hosts for
Anisakis if they consume raw or undercooked fish.1
Infection is known as anisakiasis and is often associat-
ed with gastrointestinal symptoms such as abdominal
pain, diarrhoea, nausea and vomiting. Patients’ reac-
tions range from being asymptomatic to requiring
emergency room care. Since 1960 when anisakiasis
was first described, thousands of cases have been
reported from Japan and hundreds from Europe, the
USA. and other parts of the world.2
Correspondence: Dr N Niewenhuizen, Division of Immunology,Institute of Infectious Diseases and Molecular Medicine, University of Fig. 1. Anisakis larvae removed from Thyrsites atun Cape Town, Observatory 7935. E-mail [email protected] Current Allergy & Clinical Immunology, August 2009 Vol 22, No. 3 is accompanied by allergic reactions such as urticaria, Only one case of food allergy to Anisakis has been doc- angio-oedema, bronchospasm and/or anaphylaxis.7,8 umented in South Africa28 despite the recent popularity This allergic response can occur without gastrointesti- of sushi, perhaps because the disease is largely nal symptoms, leading to misdiagnosis of the reaction unknown to physicians and may go undiagnosed.
to Anisakis as fish allergy or idiopathic urticaria/anaphy- Recently, several case reports described adverse reac- laxis.5 Symptoms can begin anywhere between a few tions to Anisakis in individuals handling fish or fishmeal, hours to more than a day after ingestion of the para- with symptoms ranging from conjunctivitis to allergic site, and patients may therefore not connect the inges- asthma.16,17,19 In an epidemiological study of two large tion of the fish to the symptoms. Although some fish-processing factories in St Helena Bay on the west patients tolerate dead larvae in frozen or cooked fish, coast of South Africa we found a prevalence of 8% others have symptoms after eating well-cooked or sensitisation to Anisakis among the fish-processing canned fish, indicating that both live and dead larvae workers,6,29 but only 1-3% had Anisakis-related allergic and their proteins can cause allergic reactions.9-12 A his- symptoms. The study also found that indviduals with tory of fish consumption prior to allergic symptoms and Anisakis sensitisation were twice as likely (OR = 2.24, the absence of sensitisation to fish indicates the need CI: 1.01-4.97) to have high seafood intake as measured to test for Anisakis allergy.
by elevated level of serum omega-3 fatty acids (eicos- Currently, the diagnosis of Anisakis allergy relies on a apentaenoic acid). We therefore decided to look at pat- clear history of potential exposure to Anisakis and terns of IgE-binding proteins recognised by our symptoms of gastroallergic anisakiasis along with sensitised workers to compare them with patterns Anisakis specific IgE and positive Anisakis skin-prick found in previous studies where patients had symp- tests (SPTs).5,7 However, because many allergens of Anisakis are heat stable, exposure to Anisakis proteins Immunoblotting using serum from 15 workers who in fish on an ongoing basis can also cause symptoms were ImmunoCAP or SPT positive to Anisakis (Table I) such as chronic urticaria, protein contact dermatitis, showed diverse patterns of IgE binding to Anisakis pro- asthma and rhinoconjunctivitis.13-19 In this case the clin- teins (Fig. 2), as has been observed in previous stud- ical history may be less clear since patients may be ies.30 Somatic Anisakis antigens were used for exposed to many agents in their environment at the immunoblotting, as the workers were likely to be same time. The use of specific IgE alone to diagnose exposed to Anisakis through handling of fish, inhalation Anisakis allergy is confounded by the fact that even of vapours and consumption of cooked fish. Workers asymptomatic individuals can have Anisakis specific who were positive to Anisakis on ImmunoCAP were IgE because of cross-reactivity with other helminths often also positive to Ascaris lumbricoides, a human (e.g. Ascaris) or invertebrates such as dust mites, cock- roundworm, which is closely related to Anisakis.31 A roaches and shrimp.20-22 Studies in Spain have found subgroup analysis of sera (n = 129) demonstrated a that a large number of asymptomatic individuals have very high correlation (r = 0.72, p <0.001) between IgE Anisakis specific IgE, some related to subclinical sensi- reactivity to Anisakis and Ascaris (unpublished data).
tisation and others due to false-positive results as a Immunoblotting against Anisakis extract may be less useful for diagnosis if the patient has a past Ascaris The muscle protein tropomyosin is an important source infection because of cross-reactivity between Anisakis of cross-reactivity with other invertebrates. Recently and Ascaris.32 We therefore looked at patterns of IgE we showed by allergen microarray analysis that all binding in workers who had a higher level of specific patients with specific IgE antibodies to Anisakis IgE to Anisakis than to Ascaris, similar levels of specif- tropomyosin (Ani s 3) also recognised tropomyosin of ic IgE to both worms, or a higher level of specific IgE to shrimp, dust mite, cockroach and snail (unpublished Ascaris than to Anisakis. Sera from three workers who data). Whether Anisakis tropomyosin is a clinically rele- were SPT positive but ImmunoCAP negative to vant allergen is however controversial. Asturias et al .20 have suggested that tropomyosin is not an important Most of the workers recognised a variety of medium- allergen as asymptomatic patients were sensitised to it molecular-weight proteins ranging from about 33 to 75 whereas symptomatic patients were not. Other kDa, including the workers who were primarily sensi- researchers suggest that Anisakis tropomyosin could tised to Ascaris. Some also recognised low-molecular- play a role in eliciting food allergy after ingestion of weight proteins, reportedly an indication of real cooked seafood, because it closely resembles the exposure to Anisakis rather than cross-reactivity to heat-stable shrimp tropomyosin, an important allergen other invertebrates.26 The IgE-binding pattern was more variable in the workers who had higher specificIgE to Anisakis than to Ascaris. One of these workers THE ROLE OF IMMUNOBLOTTING IN THE
had IgE against only two proteins of approximately 52 DIAGNOSIS OF ANISAKIS ALLERGY
and 75 kDa (with fainter binding at 37 kDa) and anoth-er recognised only a single band at about 42 kDa. A Since cross-reactivity can cause false-positives in SPTs third was strongly sensitised to a cluster of proteins and specific IgE tests, some authors have used IgE immunoblotting to differentiate anisakiasis/Anisakis Some of the IgE-binding proteins identified in our study allergy from asymptomatic Anisakis sensitisation.24,26,27 have not yet been characterised or identified as aller- One study found that patients with confirmed Anisakis gens. Previous studies have also detected IgE-binding allergy had IgE directed at several proteins of medium proteins different to the known allergens by molecular weight as well as low-molecular-weight pro- immunoblot analysis.23,30,33,34 Furthermore, up to the teins, while patients with no allergy or doubtful symp- present allergen characterisation has used sera from toms were more likely to recognise either a single patients with gastroallergic anisakiasis, and it is possi- medium-molecular-weight protein of approximately 40 ble that different proteins may be involved in occupa- kDa (possibly Anisakis tropomyosin) or a few medium- tional sensitisation through inhalation or skin contact.
molecular-weight proteins.26 Another study also found Allergen recognition is thought to vary significantly that asymptomatic blood donors with specific IgE to from patient to patient in Anisakis allergy, and patients Anisakis frequently detected a single protein of 42 kDa may also recognise cross-reactive proteins from other whereas truly sensitised patients recognised multiple invertebrates.23,30,33,34 Originally, authors used immuno- Current Allergy & Clinical Immunology, August 2009 Vol 22, No. 3 Table I. Descriptive data of Anisakis-sensitised workers whose sera were investigated by immunoblotting
Symptoms
Non-specific
Anisakis Anisakis
Ascaris
Sensitisation
Other sensitisations
broncho-hyper
ImmunoCAP
ImmunoCAP
to Anisakis
(microarray,
responsiveness
tropomyosin
ImmunoCAP*
(Ani s 3) on
microarray*
Current Allergy & Clinical Immunology Pen i 1, Pen m 1, Per a 7, Der p 10, Hel as 1 ImmunoCAP: latex, lobster, anchovy, pilchard Microarray: Api m 1, Cup a 1,Lol p 1, Ole e 1 SPT: HDM, cockroach, ryegrass, raw lobster, Aspergillus Pen i 1, Per a 7, Pen m 1,Phl p 1, Der p 10, Hel as 1 * A value greater than 0.35 kU/l was considered positive.
SPT – skin-prick test, HDM – house-dust mite.
Fig. 2. IgE immunoblotting against Anisakis antigens using sera from 15 Anisakis-sensitised fish-processing work-ers. Workers 1-4 had higher specific IgE to Anisakis than to Ascaris, workers 5-10 had specific IgE to both Anisakisand Ascaris, workers 11-12 had higher levels of specific IgE to Ascaris than to Anisakis and workers 13-15 wereSPT positive to Anisakis but negative on ImmunoCAP tests. blotting with deglycosylated Anisakis proteins or excre- The major allergens of Anisakis (recognised by more tory-secretory (ES) proteins to increase the specificity than 50% of patients) are considered to be Ani s 1 and of Anisakis diagnosis.24,33 However, to avoid misdiagno- Ani s 7,38 although in one study Ani s 5 was recognised sis due to cross-reactivity, it is ideally better to use puri- by 49% of patients (41/84). The 24 kDa Ani s 1 is recog- fied or recombinant allergens that are specific for nised by 67-87% of patients with gastroallergic anisaki- Anisakis-allergic patients.34 The identification of specif- ic Anisakis allergens which could be used in tests such individuals.23,39 This allergen is secreted by the worm as ImmunoCAP, SPT, allergen microarray or immuno- and shows homology to serine protease inhibitors. A blotting will in the long term increase the specificity of 21 kDa isoform of Ani s 1 also exists.39 Ani s 1 is heat stable and can act as a food allergen, causing reactionsafter ingestion of cooked fish. The other major allergen, ANISAKIS ALLERGENS
Ani s 7, is also an ES product of 139 kDa and is a novelglycoprotein.40 It was recognised by 100% of patients Currently nine allergens of Anisakis simplex have been with Anisakis allergy.40 However, Ani s 7 has cross- identified, most of which exist in recombinant form.
reactive O-glycans and is better for diagnostic tests Patients may be exposed primarily to somatic antigens from dead larvae in food, ES antigens when there is Another important allergen is Ani s 4, a heat-stable expulsion or surgical removal of the intact larvae, or nematode cystatin that is recognised by only 27-30% both, in cases where the larva penetrates the tissue, is of patients but appears to be particularly important in killed by the host, and subsequently degenerates eliciting anaphylaxis.9 Heat-stable allergens such as Ani inside the host.35 Many allergens of Anisakis are heat s 4 are important even if they are classified as minor and/or pepsin resistant9,36,37 and most of them are allergens as a result of their frequency of recognition, because these allergens are associated with allergic Current Allergy & Clinical Immunology, August 2009 Vol 22, No. 3 Table II. Anisakis allergens
Allergen
Molecular weight
Description
Location
Recognition in
Recombinant
Anisakis-sensitised patients
protein exists
References
specific IgE0% (0/10) patients with true Anisakis allergy Current Allergy & Clinical Immunology SPX/RAL protein Homologous with proteins in the SXP/RAL-2 family,including Ani s 5 reactions to cooked or canned fish.42 Therefore, fre- TG, Brombacher F. Exposure to the fish parasite Anisakis causesallergic airway hyperreactivity and dermatitis. J Allergy Clin quency of recognition is not always equal to clinical rel- Immunol 2006; 117: 1098-1105.
evance. Other minor allergens include Ani s 5 (15 kDa), 7. Daschner A, Alonso Giqm A, Cabanas R, Suarez-de-Parga JM, MC Ani s 8 (15 kDa) and Ani s 9 (14 kDa), which share Liqm-S. Gastroallergic anisakiasis: borderline between food allergy homology and are all members of the SPX/RAL-2 fami- and parasitic disease – clinical and allergologic evaluation of 20 ly, which is specific to nematodes. They are all heat-sta- patients with confirmed acute parasitism by Anisakis simplex. ble ES products, although Ani s 9 is reportedly more J Allergy Clin Immunol 2000; 105: 176-181.
abundant in crude extract, and their biological function 8. Audicana MT, Fernandez de Corres L, Munoz D, Fernandez E, Navarro JA, del Pozo MD. Recurrent anaphylaxis caused by is unknown.36,42,43 Another minor allergen, Ani s 6 (7 Anisakis simplex parasitizing fish. J Allergy Clin Immunol 1995; 96:
kDa), is homologous with serine protease inhibitors, including the honeybee allergen Api m 6.34 9. Moneo I, Caballero ML, Gonzalez-Munoz M, Rodriguez-Mahillo AI, The remaining two allergens, Ani s 2 (41 kDa) and Ani Rodriguez-Perez R, Silva A. Isolation of a heat-resistant allergen
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MANAGEMENT OF ANISAKIS ALLERGY
18. Carretero Anibarro P, Blanco Carmona J, Garcia Gonzalez F, et al. The ideal diagnostic test for Anisakis allergy should Protein contact dermatitis caused by Anisakis simplex. Contact
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canis. Mol Biochem Parasitol 1988; 31: 35-46.
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Declaration of conflict of interest
25. Guarneri F, Guarneri C, Benvenga S. Cross-reactivity of Anisakis The authors declare no conflicts of interest.
simplex: possible role of Ani s 2 and Ani s 3. Int J Dermatol 2007;
46: 146-50.
Acknowledgements
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National Research Foundation of South Africa and an Allergy Society of 27. Del Pozo MD, Moneo I, de Corres LF, et al. Laboratory determina- South Africa (ALLSA) research award.
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