Route Of Exposure

The phylum Mollusca comprise about 100 000 different species, including several important seafood groups such as mussels, oysters, abalone, snails, clams, octopus, and scallops and squids. The phylum is typically divided into nine or ten taxonomic classes, of which two are entirely extinct. The most important divisions of the phylum Mollusca are the classes Bivalvia (bivalves such as clams, mussels, oysters, and scallops), Cephalopoda (cephalopods such as cuttlefish, octopus and squid) and Gastropoda (gastropods such as abalone, limpets, snails, winkles and whelks). Members of other classes of molluscs such as chitons are also sometimes eaten. Marine molluscs and crustacea (shrimps, prawns, crabs, crayfish and lobsters) are both known as shellfish. (‘Mollusk’ is the American spelling and ‘mollusc’ the British spelling).

Abalone are marine ‘snails’. The family Haliotidae contains only one genus, Haliotis, which contains between 4 and 7 subgenera. The number of species worldwide ranges from about 100 to 130. The Haliotid family has a worldwide distribution, being found in at least some areas along the coastal waters of every continent, except the Atlantic coast of South America, the Caribbean, and the East Coast of the United States. Most abalone are found mainly in cold waters, off the southern hemisphere coasts of New Zealand, South Africa and Australia, and off western North America and Japan in the northern hemisphere.

The family has unmistakable characteristics: the shell is rounded to oval, with two to three whorls – the last one auriform (grown into a large ‘ear’), giving rise to the common name ‘ear-shell’. Abalone shells have a low and open spiral structure. Colour is variable from species to species. An abalone clings solidly to rocky surfaces with its muscular foot, at sublittoral depths.

The innermost layer of the shell is composed of nacre or mother-of-pearl, which in many species is highly iridescent, giving rise to a range of strong and changeable colours, and causing abalone to be harvested for use as decorative objects. The iridescent mother-of-pearl can vary in colour from silvery white or pink to red and green-red, through to ‘Haliotis iris’, which shows predominantly deep blues, greens and purples.

Abalone is characterised by several respiratory holes in a row near the shell's outer edge (anterior margin). These number from 4 to 10, depending on the species.

The meat of Abalone (the thick muscle with which they attach themselves to rocks) is considered to be a delicacy. Size varies from 20 mm (H. pulcherrima) to 200 mm, or even more (H. rufescens). Although molluscs are eaten all over the world, the species eaten and the quantity consumed differ greatly from region to region. Abalone is normally eaten as a cooked dish. It may be found in soups or Chinese dishes such as dim sum. It is sometimes used in rice porridge; but this is not common, as it is one of the most expensive shellfish.

Clinical Relevance

Allergen Description

A number of allergenic proteins have been isolated. Two major allergens with molecular weights of 38 and 49 kDa were consistently identified using sera from 5 of the 7 abalone-allergic individuals tested, the latter IgE-binding protein designated as Hal m 1. Higher molecular mass (50 to 70 kDa) allergens were also observed. However, unique allergens may be present in each species of abalone.

Allergens characterised to date:

Abalone allergens are heat stable, as are other mollusc allergens.

Similar allergens have been characterised or isolated from other species of abalone, e.g. Hal di 1 (H. discus) and Hal d 1 (H. diversicolor), as well as a heat shock protein from H. discus.

Tropomyosin has been identified as a mollusc allergen in abalone (species not known), scallop and mussel. In addition, tropomyosin has been isolated from Japanese abalone (H. diversicolor), red abalone (H. rufescens), and tropical abalone (H. asinina).

Tropomyosin is heat stable, yet its allergenicity may change as a result of certain processing methods. Boiling may result in the Maillard reaction (glycation) and formation of neoepitopes, as demonstrated in some patients, for whom boiled shrimp extract induced larger skin-test responses than raw extract. Also, shrimp extract treated with high intensity ultrasound for 180 minutes demonstrated decreased binding with sera from shrimp-allergic patients. (12, cited in 13)

Potential Cross Reactivity

Cross-reactivity between different species of abalone is likely. Immunoblots with extracts from the abalone H. rubra, together with cooked or dried H. midae, gave similar IgE-binding patterns to those with raw H. midae.

Allergy to abalone is most often associated with allergy to other related molluscs. Cross-reactions are found between molluscs, especially within the same class (bivalves, cephalopods or gastropods). Thus those allergic to bivalves (clams, mussels, oysters, and scallops) are likely to react to other bivalves, while those reacting to gastropods (abalone, limpets, snails, winkles and whelks) are likely to react to other gastropods.

However, demonstration of sensitisation to a specific abalone allergen may be more indicative of the next-closest cross-reactive species or food.

This is illustrated by a study that consistently identified two major allergens (38 and 49 kDa (Hal m 1)) from the sera of 5 of 7 abalone-allergic individuals tested. IgE from the sera of abalone-allergic patients also bound to proteins from snail, white mussel, black mussel, oyster, and squid. The main IgE-binding protein from mussel had a molecular mass of 38 kDa, and a protein from oyster at 38 kDa also bound IgE.

Similarly, strong IgE-cross-reactivity was demonstrated between common whelk (Buccinum undatum) and (taxonomically, closely-related) abalone by ELISA inhibition. No cross-allergenicity was found with shrimp or house-dust mite.

A study on a patient who experienced fatal anaphylaxis following consumption of 3 terrestrial snails noted that the patient had previously been diagnosed as allergic to abalone. Significant cross-reactivity was demonstrated between abalone and limpet, based on skin-prick results. However, the ‘limpet’ species was not well defined.

In general, allergy to crustacea (shrimps, lobster, crayfish, or crab) is due to the highly conserved muscle protein tropomyosin. Tropomyosin is not only a major crustacean allergen but is found in a number of mollusc species, including abalone. In contrast to invertebrate tropomyosin, vertebrate tropomyosins are not allergenic: individuals with a history of meat allergy have not shown any IgE binding to tropomyosin of beef, pork, rabbit or chicken, and similarly, serum-specific IgE from shrimp-allergic subjects did not cross-react with any mammalian tropomyosins. (16, 20, cited in 13)

Importantly, therefore, although in vitro studies show that IgE antibodies from shrimp-allergic patients also frequently bind to tropomyosins from molluscs, this does not necessarily demonstrate clinical allergy. Positive skin-prick tests with shrimp were associated with a 26% to 41% probability of a positive skin test to scallop, clam, oyster, abalone or limpet. Indeed, little cross-reactivity has been demonstrated between abalone and many other crustacean allergens. As tropomyosin is also involved in cross-reactivity between insects and crustaceans, it is possible that individuals with allergy to cockroaches and other arthropods might show cross-reactions with molluscs: but this may be clinically irrelevant, i.e. no symptoms may be experienced.

This is supported by a study that demonstrated that although tropomyosin is the major allergen among various common edible molluscs, a comparison of the amino acid sequences of epitopes in crustaceans and molluscs suggested that the epitopes in the two groups may be distinct. This is supported by other studies.

However, a study assessing the amino acid sequence of the acorn barnacle (Balanus rostratus) tropomyosin found it to be more homologous (76 to 78%) to those of abalone tropomyosins (Japanese abalone (H. diversicolor), red abalone (H. rufescens), and tropical abalone (H. asinina)) than to those of decapod tropomyosins.

One common practice is to substitute abalone with limpet – this needs to be borne in mind.

Clinical Experience

IgE-mediated reactions

One of the first case reports of allergy to abalone was described in 1979, for individuals with acute respiratory hypersensitivity to abalone. Subsequent to that, a number of studies have characterised the nature of allergy to abalone. Adverse reactions following the ingestion of abalone range from mild oral allergy syndrome, through urticaria (which is probably the most commonly-reported symptom), to life-threatening systemic anaphylaxis. Symptoms may involve nausea, diarrhoea, and asthma or rhinitis. Most symptoms occur within 90 minutes of ingesting the food, but delayed reactions have also been reported. Although symptoms generally occur after ingestion of abalone, symptoms have been reported on handling or inhaling steam from cooking molluscs, and asthma has been associated with workers opening mussels, suggesting that similar reactions may occur with abalone. Indeed, occupational asthma from inhalation of abalone vapour in an abalone fisherman has been reported. Severe symptoms sometimes only occur when exercise follows shortly after eating abalone.

A number of case reports have described possible adverse reactions to abalone.

An Australian report described immediate respiratory hypersensitivity to abalone occurring in two individuals. An abalone fisherman developed asthma on contact with abalone – a bronchopulmonary inhalational challenge with an abalone extract made from viscera and muscle resulted in a 45% fall in FEV1. The second patient, an asthmatic female sensitised to house-dust mite, noticed that when she came near abalone she experienced hay fever and exacerbation of her asthma. Her daughter occasionally worked at cleaning abalone, which coincided with when she experienced these symptoms. A skin-prick test to abalone extract was positive.

Anaphylaxis was reported to have resulted from abalone in a 30-year-old man, who described generalised oedema, dyspnoea and urticaria occurring immediately after eating raw fish and cuttlefish served on an abalone shell. He had a history of anaphylaxis after eating abalone and beef 4 years prior to this episode, and had avoided shellfish (including abalone) since then. He had also previously experienced bronchial asthma and anaphylaxis due to shrimp. Serum-specific IgE was shown for scallop and oyster. As commercial extracts were not available for skin and serum IgE testing, skin-specific IgE tests were performed with lab-manufactured extracts, and were positive for abalone and for the effluent from washing the abalone shell.

A South African study recruited 105 volunteer subjects with suspected fish allergy, by advertising in the local press. The four most common seafood species reported to cause adverse reactions were prawns (46.7%), crayfish (43.8%), abalone (35.2%) and black mussels (33.3%). Symptoms were not listed by food, but it was noted that abalone caused several severe reactions.

A secondary article on a subset reported that 45% of subjects (18 of 38) with seafood allergy had specific IgE to an indigenous abalone species, H. midae. Fourteen of 24 patients were skin-prick test-positive for abalone, 9 of 24 for oyster, 10 of 24 for black mussel, 6 of 24 for blue mussel, 5 of 24 for white mussel and 7 of 24 for squid. Twenty-five of the 38 patients in the study were first seen with immediate symptoms, and 13 had delayed reactions. Symptoms of the 38 patients were divided into four categories: cutaneous, gastrointestinal, respiratory, and ‘other’. Although most of the subjects (66%) reported symptoms within 2 hours of food ingestion, a significant number of subjects (13, or 34%) reacted only between 2 and 7 hours after eating. In both groups the majority of the subjects (76% and 69%, respectively) experienced cutaneous and respiratory symptoms, whereas the remaining subjects were first seen with gastrointestinal symptoms. Skin-prick tests with abalone extract were positive in all subjects with positive RAST (n = 8) and in 6 of 13 subjects with negative RAST. Five of the subjects with positive RAST were confirmed with Western blotting with demonstration of two major allergens of 38 and 49 kDa. Clinical and immunologic heterogeneity in patients reactive to abalone was found.

A Japanese study described 11 individuals who developed moderate to severe anaphylactic reactions following the ingestion of grand keyhole limpet and abalone, confirmed by history, skin-prick test, RAST and immunoblotting. Only 1 patient reacted to haemocyanin. RAST inhibition studies demonstrated cross-antigenicity between limpet, abalone and keyhole limpet haemocyanin. What appears to be a subset of 5 patients of this study was reported on elsewhere. Of the 5 abalone-allergic individuals, 2 reacted only 90 minutes to 3 hours after eating.

A single case of exercise-induced anaphylaxis to abalone was described in a study of 11 Japanese patients with food-dependent, exercise-induced anaphylaxis.

Few studies have evaluated the prevalence of abalone allergy.

A report of anaphylaxis in adults referred to a Singapore clinic found that ingestion of molluscs (abalone and limpet) was the most common cause of food-related anaphylaxis (11 of 30 cases).

As mentioned above, a South African study of individuals with self-reported hypersensitivity to seafood (which included fin fish and crustacean) reported that reaction to abalone (also called perlemoen) was the third most common reaction to seafood after reaction to shrimp and crayfish, with 38 of 105 patients reacting to abalone.

In a study to determine the clinical characteristics of shellfish-allergic patients in Hong Kong and the pattern of skin-test reactivity, 84 consecutive patients attending an allergy clinic of a large teaching hospital for suspected shellfish allergy were evaluated. Twenty-eight patients reported a history of severe anaphylaxis. Fourteen patients had no positive shellfish skin test (7 of whom presented with anaphylaxis after shellfish ingestion), and were excluded from further analysis. Overall, 43 patients claimed they had reactions to shrimp, 37 to crab, 11 to lobster, 1 to scallop, 6 to limpet, 5 to abalone, 3 to snail, 1 to mussel, and 1 to clam. There were 183 positive shellfish skin tests, with an average of 2.61 positive tests per subject. Seventy patients were SPT positive to a shellfish, and 45 patients were sensitised (i.e. SPT positive) to abalone and/or limpet; 27 of these were also sensitised to crustacea. Limpet gave more positive SPTs (40%) than abalone (26%). Ninety percent of subjects also had positive skin tests to house-dust mites. Sensitivity between limpet and abalone was significantly interdependent. However, the ‘limpet’ species was not well defined. One of the patients, known to be allergic to abalone, suffered fatal anaphylaxis recently after ingesting three snails.

A questionnaire study of 1 510 Japanese families, to which 878 families responded (1 383 patients, 402 having previously experienced anaphylaxis), implicated 6 549 allergens. Egg, milk, wheat, peanuts, and buckwheat were the most common food allergens. A total of 81 patients reported allergy to abalone, none being mono-sensitised. Using statistical analysis, the authors suggested that the occurrence probability of a combination (i.e. a person presenting with allergy symptoms to a certain allergen and simultaneously presenting with allergy symptoms to another allergen), called 'confidence', was higher for 'chicken-egg', 'abalone-salmon eggs', and 'matsutake mushroom-milk', in that order. From the results of the association analysis, the authors speculated that some food allergens – such as abalone, orange, salmon, chicken, pork, matsutake mushroom, peach and apple – did not induce food reactions independently.

Other reactions

The calcium carbonate dust created through the grinding and cutting of abalone is a respiratory irritant, and the particles can penetrate into the lower respiratory tree and cause irritant bronchitis and other respiratory irritation responses. Proteins left in the shell matrix may trigger an allergic reaction.

Two Japanese reports, predating 1970, suggest that a “severe form of photosensitivity” can arise from eating the liver of abalone. (41, 42, cited in 23)

Scombroid poisoning (histamine reaction) is usually associated with tuna, mahi-mahi, bluefish, sardines, mackerel, and amberjack; however, a single reference (not corroborated) suggests that it may also be associated with ingestion of abalone.