A. Case study
B. More information
C. Editors' comments
E. CPD questions (South Africa, Australia)
A. Case study
A 40-year old man
experienced a couple of episodes of acute, generalized urticaria within
minutes of having a meal that included tuna. He had eaten tuna before
on many occasions without any adverse reactions and therefore assumed
that it was something else in the meal that caused the reaction. He
continued to eat tuna after that and did not experience urticaria every
time. In total, he reacted 3 times after the initial reaction and twice
failed to react. This occurred over a period of 20 months and involved
more or less the same amount of tuna every time. He did not react to
physical contact with fish and did not eat canned tuna.
The patient had
never shown any type of reaction to any other fish species. His wife,
being a dietitian, monitored his dietary intake carefully, trying to
determine whether there was a correlation between his dietary intake
and the reactions.
What could be the possible causes for his reaction?
a. He was reacting to the tuna.
b. He was reacting to something else in the meal.
c. He was reacting to something in the environment while he was eating
The wife could not
pick up any other element than tuna in the meal that was consistently
associated with the reaction. Also, the environment could not give any
clues. Three out of the 4 reactions occurred after eating tuna in a
specific restaurant, but he also ate tuna there without any reaction.
Could one react to tuna on one occasion and not the next? What type
of reaction could it be? An allergy, intolerance or toxic reaction?
a. He was reacting to a heat-labile allergen in tuna. The fish may not
have been cooked through on the occasions that he reacted to it.
b. The fish he was eating was not always tuna (although he thought it
was), i.e., he was truly allergic to tuna, but at the times he did not
react to the "tuna", he was eating another type of fish.
c. The preparation method was not always the same (e.g., on some occasions
spices were added, and these caused his reaction).
d. He reacted to histamine in tuna, as histamine intolerance can present
with allergy-like symptoms. The fish may not have been stored properly
on the occasions that he reacted to the tuna, so as to have increased
levels of histamine.
e. Whatever induced his reaction (e.g., bacteria or toxin) was "contaminating"
the fish and would therefore not always be present in all tuna.
a. This could be possible. To determine if it was the case, a serum-specific
IgE test to tuna could be done.
b. This was not the case.
c. This was not relevant.
d. If the patient was sensitive to histamine and he had not reacted
to other histamine-containing foods before, it would indicate that he
reacts to a high dose of histamine. On the occasions that he reacted
to tuna, the fish could have contained high levels of histamine (indicating
that it had been improperly stored). But the restaurant owner claimed
that the fish that he served were freshly caught and served. This possibility
was thus excluded.
e. If he were reacting to a contaminant, then others eating the same
meal in the restaurant would also have been affected.
It was decided to
measure his total IgE and serum-specific IgE test to tuna. The total
IgE was increased, but the IgE to tuna was normal.
What did this indicate?
He was definitely sensitized to something, but it was not tuna. The
wife decided to contact specialists in the field and was told to consider
an allergy to Anisakis simplex. Allergy to this fish parasite is quite
common and is difficult to distinguish from regular allergy to fish.
A serum-specific IgE test to this parasite was performed and confirmed
|TIP for Allergy
Allergy Advisor would been useful in the assessment of this
patient. Entering "fish" into the search function
of Allergy Advisor will bring up information, for example
that Anasakis simplex and other contaminants may be present
and could be the cause of a reaction. Looking under "tuna"
specifically, the following information could be obtained:
"Possible additional constituents" indicate that
there is an association with tuna and histamine/scromboid
poisoning, tartrazine can be present in canned tuna even though
it is not labeled as such and reactions are possible to raw
and cooked tuna. From there one could find more information
on histamine, etc.
B. More information:
Many people associate
adverse reactions to fish only with allergy. But there are in fact many
types of reactions to fish, including (see lettered sections, here indicated
in parentheses, for more information):
- Allergy to
allergens inherent in the flesh of fish
- Allergy to
parasites present in fish, e.g., Anisakis simplex (a)
- Allergy to
iodine, of which fish is a rich source of (b)
- Histamine sensitivity/scromboid
substances, e.g., wax esters in certain species of fish (d)
- Toxic reactions:
- Ciguetera poisoning
- Heavy metal
toxicity, e.g., methyl mercury (f)
- Parasitic infestation,
e.g., Anisakis simplex (a)
- Bacterial and
viral contamination, e.g., salmonella (g)
will give a brief overview of some of these reactions other than the
regular fish allergy. Some of the topics are discussed in more detail,
according to how common the problems are and how much is known about
ADVERSE REACTIONS TO ANISAKIS SIMPLEX
Anisakis simplex or cod worm is a seafood-borne parasite that can cause
two major problems in humans: infection (anisakiasis) and allergic reactions.
Various studies have shown that 5-80 % of fish samples are infested
by Anisakis (mainly freshwater fish). It first inhabits the gut of the
fish, but migrates into other tissues when the fish's temperature rises
as a result of storage conditions.1,2
Adverse reactions have been recorded to ingesting or inhaling the Anisakis
allergen(s) due to an IgE-mediated allergic reaction.3 A study in
Spain found that allergy to Anisakis was more frequent than fish allergy
and sensitization much higher.4 Allergic reactions to this parasite
should be suspected when allergic-like reactions occur after eating
seafood, yet the results of serum-specific tests to seafood are normal.
Reactions often occur intermittently after eating seafood rather than
on every occasion.
-20 degrees Celsius for more than 48 hours and cooking at temperatures
higher than 60 degrees Celsius for 10 minutes is important in protecting
against infection with live parasites, but may not protect against reactions
to their allergens.5,6 The heat-stability of Anisakis allergens has
been demonstrated,7 even though there have been reports of sensitized
individuals (with a history of severe allergic disease to the parasite)
who did not react to the dead larvae.2 The clinical reality is that
sensitized individuals may react to cooked, frozen or canned fish.7
that have been reported include urticaria, angiodema, anaphylaxis, asthma,4,7,8,9
and eczema.10 Occupational exposure upon inhaling particles of Anisakis
simplex (through cutting fish and inhaling fish flour) have been recorded
to cause conjunctivitis (perennial itching, burning and redness of eyes
with increased tearing)11 and asthma.12
If an individual is infected by this parasite, it can lead to anisakiasis
or anisakidosis (herring or cod worm disease)13, an acute or chronic
disease involving mainly the digestive tract. It only affects those
who consume raw or undercooked parasitized fish.3 As noted, deep-freezing
or cooking infected fish at appropriate temperatures is necessary to
protect against infection.6
Fish is a good dietary source of iodine. Fish allergy and iodine allergy
are independent of each other.
Histamine is a vasoactive amine that can induce allergy-like symptoms
in sensitive individuals. The reactions, however, are not IgE-mediated,
but of an intolerance type reaction.14
Histamine may occur
naturally at different concentrations in some foods such as fish, wine
and cheese. The level present in fish can increase when fish is improperly
refrigerated or refrigeration is delayed (even though the fish is not
rancid). Histidine (naturally present in fish) is converted by histidine
decarboxylase to histamine at an optimal temperature of 20-30 degrees
Celsius. The longer fish is improperly stored and remains ungutted,
the higher the histamine content.15,16,17 Fish involved include mackerel,
tuna, herring, sardines, marlin, anchovies and bluefish. Affected fish
often have a metallic or peppery taste.18
in freshly-caught fish are less than 1mg/100g of fish, but if the fish
is left at room temperature can increase to up to 100mg histamine/100g
of fish within 12 hours.17 Hazardous levels are thought to be 50mg
histamine/100g or more.16 But it is important to note that high levels
of histamine do not necessarily occur in fish that are rancid.
The term "scromboid
poisoning" originates from the fact that spoiled fish from the
family Scombridae (e.g., tuna, mackerel and bonito) were originally
implicated in incidents of this type of poisoning. But it is not the
only fish that can cause histamine reactions.16,17,19
Some studies have
shown that histamine-intolerant individuals have a deficiency of the
enzyme, diamine oxidase, in the jejunal mucosa, resulting in diminished
histamine degradation and absorption in the gastrointestinal tract.
In pregnancy, diamine oxidase levels are known to be about 500-fold
elevated.20 Up to 94 drugs have been shown to inhibit diamine oxidase,
including dihydralazine, isoniazid, clavulanic acid, promethazine, verapamil
and metoclopramide. Alcohol is seen as a histamine liberator, i.e.,
it can enhance the effect of histamine in sensitive individuals.21
The onset of the
symptoms usually occurs within a few minutes after ingestion of the
food, and the duration of symptoms ranges from a few hours to 24 hours.
Reactions that have been recorded to histamine are flushing, headache,
dizziness, burning sensation in the mouth and throat, peppery taste,
abdominal cramps, nausea, vomiting, diarrhoea, urticaria, generalised
pruritis, sneezing, bronchospasm, asthma, respiratory distress, hypotension
and eczema.17,22 Histamine has also been implicated as an important
mediator in certain types of headaches that are thought to differ from
migraine and tend to be located to one side of the head and face.15
WAX ESTERS IN FISH
The passage of oil through the rectum has been observed following the
ingestion of "butterfish": a food idiosyncrasy. There have
only been a few articles in the literature on this subject: 1 in a South
African journal23 and 3 in one issue of Communicable Diseases Intelligence
in 200224,25,26. The latter journal's articles reported 3 "outbreaks"
in Victoria. There has also been one similar communication from New
South Wales in October 2001. Following media reports on this issue in
Australia, there have been numerous additional reports (60 before 2002).27
Dr. Harris Steinman
(one of the editors of this newsletter) has, while lecturing, asked
his audience on several occasions how many of them have experienced
this before. Around half would put up their hands. There is probably
a significant under-reporting of this condition, as the symptoms can
be mild and short-lived.27 But for some affected individuals, they
can be quite dramatic and embarrassing (as discussed below). Also, the
incidence is likely to be increasing as butterfish is eaten more commonly.
In the studies,
there is some confusion about the correct names of the fish that cause
this passage of oil per rectum. The following points have to be considered:
"Escolar", "oilfish" and "rudderfish"
have been marketed and sold as "butterfish";
Reactions have been associated with "escolar", "oilfish",
"rudderfish" and "Lepidocybium flavobrunneum," the
latter given as the scientific name for butterfish when this is in fact
"Escolar" is sometimes given as a collective name
for true escolar and oilfish.
One study showed that true rudderfish (Centrolophus sp., and
Tubia sp.) is not a cause, only escolar (L. flavobrunneum) and oilfish
Escolar and rudderfish are deep-water fish, whereas butterfish
are found in more-shallow waters.27
To illustrate the
similarities between Ruvettus pretiosus, Lepidocybium flavobrunneum,
Centrolophus niger and Tubbia sp. (provided by Don Nichols of the West
Australian Seafood Quality Management Initiative):
|Figure 1. Oilfish,
||Figure 2. Escolar,
|Figure 3. Rudderfish,
||Figure 4. Rudderfish,
In one article,
a study was performed in which two of the authors consumed about 500g
each of the baked flesh of the fish. After 12 symptom-free hours, oil
began to be passed per rectum. It was difficult to contain the oil that
was pooling in substantial quantities in the lower rectum, and therefore
frequent evacuation was required. These calls of nature were generally
prophylactic visits to avoid soiling of clothing, and were not for the
most part caused by sheer inability to retain rectal contents. Or this
was, at any rate, the testimony of the subjects.23
of pure oil was passed per occasion. The oil was a clear orange or green
in colour. It was inoffensive and mostly not contaminated significantly
by faecal material. Because most experiences occurred in the absence
of any bowel cramps or abdominal discomfort, this would imply that the
frequent calls to stool were caused by the lubricant effect of the oil,
and not by an irritant action. This could therefore not be diarrhoea,
theoretically. Diarrhoea is defined as a more rapid passage and fluidity
of faecal material. The name keriorrhoea was given (the greek word,
keras, meaning "wax" and diarrhein meaning "to flow through").23
The symptoms described in other articles show wide variation. Symptoms
ranged from mild and rapid passage of oily yellow or orange droplets,
to severe diarrhoea with abdominal pain, nausea, headache and vomiting.
In those who are susceptible, the onset of symptoms occurs at a median
of 2.5 hours and within a range of 1 to 90 hours after consumption.
Most people recovered within 24 hours.24,26,27
Why does this
Escolar (this name may refer to oilfish as well: see above) and true
rudderfish contain very high levels of oil (generally between 14 to
25% of wet mass) in the fillet. Escolar oil contains mainly wax ester
(>90% of oil). The oil from rudderfish contained mainly diacylglyceryl
ether (DAGE, >80% of oil) or hydrocarbon (>80% of oil, predominately
The oil composition
of fish fillet samples was consistent with culprit foods being escolar
rather than rudderfish species. Even though rudderfish species contain
similar proportions of oil, they do not contain the indigestible wax
ester seen in escolar and oilfish.27 The high proportion of wax esters
in the flesh of the fish, their resistance to digestive enzymes, and
their low melting point all contribute to the pooling in the rectum
of significant volumes of oil. And it is the oil's lubricant quality
that then causes the frequency of stooling.23
Wax esters consist
of fatty acids esterified to similarly long-chain alcohols. Such compounds
are found in animal, plant and microbial tissues and they have a variety
of functions, such as energy storage, waterproofing and even echo-location.
The ultimate source of the wax esters (or at least the fatty alcohol
component) is likely to be zoöplankton. Most predators of zoöplankton
such as the herring, sardine and baleen whale do not accumulate wax
esters. It has been presumed that these animals cannot metabolise the
wax esters. Other wax-accumulating vertebrates are the coelacanth (Latimeria
chalumnae) and the sperm whale.23
There are little
data available to identify people susceptible to this type of oily diarrhoea.
One study could find no association between the development of the symptom
and body mass index, age or general health status. Researchers found,
however, that individuals with bowel problems, malabsorption or pregnancy
may be at increased risk. It is also possible that seasonal and geographic
differences may influence the level of indigestible wax ester content
Despite the majority
of effects being mild, warnings have been released in some jurisdictions
indicating that these fish are not suited for catering and should be
avoided by those in the high-risk category. Those eating the fish for
the first time should be advised to, initially, consume small portions
to determine their susceptibility.27
There have been
reports of toxic effects in experimental animals but not in humans.
Although many who experience this phenomenon are concerned by its effects
(including social embarrassment and having to throw away clothes soiled
with the oil), the condition appears to be medically harmless with the
quantities that are normally consumed.23
Ciguetera poisoning is triggered by eating tropical reef fish that have
fed on toxic algae, which produce a neurotoxin. This poisoning causes
more human illnesses than any other seafood toxicity. As larger reef
fish feed on smaller ones, the toxin concentrates in the organs of larger
fish such as red snapper, barracuda, sea bass, eels and kingfish. Because
the toxin is heat-stable, it is unaffected by cooking. Symptoms of this
neurotoxin present primarily as an acute neurologic disease with gastrointestinal
symptoms. Most people recover within a few days or weeks with supportive
treatment, but ongoing disability has occasionally been described.13,18
HEAVY METAL TOXICITY
Although several metals can accumulate in fish, mercury is the most
common. Mercury is a naturally occurring element, found in soil and
rocks and also in lakes, streams and oceans. It is also released into
the environment by human activities. The mercury in lakes, streams and
oceans can be transformed by bacteria into methyl mercury, an organic
and more toxic form. This form of mercury is the predominant form present
in the flesh of fish, and humans are exposed to it when ingesting the
fish. High levels of mercury can damage the nervous system, but the
effects of trace amounts are not known. Long-term studies are being
conducted to determine the effects of low levels of mercury, especially
in young children.29,30
mercury tends to concentrate or "bioaccumulate" through
the food chain, predator fish species tend to have higher levels
than non-predator fish species. In some countries the public is
advised to limit consumption of shark, marlin, swordfish and fresh
and frozen tuna. Pregnant women, women of childbearing age and young
children should limit their intake even more.29,30
Seafood poisoning outbreaks have frequently been associated with bacterial
contamination (such as Salmonella) of shellfish harvested in waters
containing untreated sewage.13
||compiled by Karen du Plessis
Food & Allergy Consulting & Testing Services (FACTS)
PO Box 565
Comments by our editor
M. Joneja Ph. D., RDN
This case study and its discussion address an important aspect
of adverse reactions to foods - namely that not all reactions
that appear to be due to food allergy are caused by an IgE-mediated
response. Symptoms such as urticaria that are thought to be typical
of allergy can in fact be due to an intolerance of histamine.
This reaction is distinct and separate from that caused by the
response to histamine released from mast cells, which is an essential
step in an allergic reaction. In addition, it is not always the
most obvious food that is responsible for triggering the production
of IgE - in this case it was the fish parasite that proved to
be the culprit allergen. Furthermore, even when there is definitive
evidence of food-specific IgE, consumption of the culprit food
does not always lead to symptoms of allergy.
In the Allergy
Nutrition Clinic at Vancouver Hospital I experienced an interesting
example of this. A patient had experienced two episodes of anaphylaxis
requiring emergency hospital treatment. The episodes occurred
two and a half years apart. On both occasions skin tests had demonstrated
a strong positive reaction to shellfish. However, the patient
was reluctant to believe that this was the cause of her reactions
since she had eaten large quantities of seafood throughout her
life, and in fact had eaten such food with impunity in between
the two life-threatening reactions. Because the second episode
had been extremely frightening for her, she came to the Clinic
to investigate what precautions she should take to prevent a recurrence.
On questioning it became clear that there were important similarities
associated with onset of her symptoms on the two occasions in
question. She had been dining in a restaurant with friends, had
eaten a large quantity of raw shellfish in the form of sushi,
had taken a moderate quantity of wine with the food, and had felt
quite well after the meal. The party moved on to a nightclub,
where more alcohol had been consumed. The patient experienced
the onset of symptoms, which included progressively more severe
urticaria, throat tightening, and shortness of breath, while dancing.
In this case, the combination of the allergenic food, alcohol,
and vigorous exercise had resulted in life-threatening symptoms,
whereas mere consumption of the allergenic food, even with concomitant
intake of alcohol, was insufficient to trigger the response.
For more information
on this subject and other allergy and intolerance related topics, visit:
To join a professional
food allergy discussion list where this subject can be discussed further,
go to http://groups.yahoo.com/group/AllergyDietitian
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" as the subject.
1. Ikeda K, Humashio
R, Kifune T. Nine cases of acute gastric anisakiasis. Gastrointest Endosc
2. Valinas B, Lorenzo S, Eiras A, Figueiras A, Sanmartin ML, Ubeira
FM. Prevalence of and risk factors for IgE sensitization to Anisakis
simplex in a Spanish population. Allergy 2001;56(7):667-71.
3. Moneo I, Caballero ML, Gomez F, Ortega E, Alonso MJ. Isolation and
characterization of a major allergen from the fish parasite Anisakis
simplex. J Allergy Clin Immunol 2000;106(1):177-82.
4. Del Pozo MD, Audicana M, Diez JM, Munoz D, Ansotegui IJ, Fernandez
E, et al. Anisakis simplex, a relevant etiologic factor in acute urticaria.
5. Audicana L, Audicana MT, Fernandez de Corres L, Kennedy MW. Cooking
and freezing may not protect against allergenic reactions to ingested
Anisakis simplex antigens in humans. Vet Rec 1997;140(9):235.
6. Audicana MT, Fernandez de Corres L, et al. Recurrent anaphylaxis
caused by Anisakis simplex parasitizing fish. J Allergy Clin Immunol
7. Montoro A, Perteguer MJ, Chivato T, Laguna R, Cuellar C. Recidivous
acute urticaria caused by Anisakis simplex. Allergy 1997;52(10):985-91.
8. Estrada Rodriguez JL, Gozalo Reques F. Sensitization to Anisakis
simplex: an unusual presentation. Allergologia et Immunopathologia 1997;25(2):95-7.
9. Fernandez de Corres L, Audicana M, et al. Anisakis simplex induces
not only anisakiasis: report on 28 cases of allergy. J Investig Allergol
Clin Immunol 1996;6(5):315-9.
10. Conde-Salazar L, Gonzalez MA, Guimaraens D. Type I and Type IV sensitization
to Anisakis simplex in 2 patients with hand eczema. Contact Dermatitis
11. Anibarro B, Seoane FJ. Occupational conjunctivitis caused by sensitisation
to Anisakis simplex. J Allergy Clin Immunol 1998;102:331-2.
12. Armentia A, Lombardero M, Callejo A, Martin Santos JM, et al. Occupational
asthma by Anisakis simplex. J Allergy Clin Immunol 1998;102(5):831-4.
14. Taylor SL. Histamine food poisoning: toxicology and clinical aspects.
Crit Rev Toxicol 1986;17(2):91-128.
15. Joneja JV. Dietary management of food allergies and intolerances
- a comprehensive guide 2nd edition. J.A. Hall Publications Ltd., USA,
16. Sanchez-Guerrero IM, Vidal JB, Escudero AI. Scromboid fish poisoning:
A potentially life-threateninng allergic-like reaction. J Allergy Clin
17. Muller GJ, Lamprecht JH, Barnes JM, et al. Scombroid poisoning.
Case series of 10 incidents involving 22 patients. S Afr Med J 1992;81(8):427-430.
19. Taylor S, Stratton J, Nordlee J. Histamine poisoning (scromboid
fish poisoning): An allergy-like intoxication. Clin Toxicol 1989;27:225-240.
20. Jarisch R, Wantke F. Wine and headache. Int Arch Allergy Immunol
21. Serghini-Idrissi N, Ravier I, Aucouturier H, Ait Tahar H, Sonneville
A. Food allergy in the chronic alcoholic and alcohol in food allergy:
apropos of 38 cases. [French] Allerg Immunol (Paris) 2001;33(10):378-82.
22. Wantke F, Hemmer W, et al. Histamine in wine. Bronchoconstriction
after a double-blind placebo-controlled red wine provocation test. Int
Arch Allergy Immunol 1996;110(4):397-400.
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per rectum - after ingestion of marine wax esters. S Afr Med J 1981;59(22):791-2.
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Victoria. Commun Dis Intell 2002;26:439-440.
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Commun Dis Intell 2002;26:440.
26. Yohannes K, Dalton CB, Halliday L, Unicomb LE, Kirk M. An outbreak
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Questions (South Africa, Australia)
ALL THE QUESTIONS
(There is only
one correct answer per question.)
1. How can one become exposed to Anisakis simplex?
(a.) Ingesting raw fish containing Anisakis simplex.
(b.) Ingesting cooked fish containing Anisakis simplex.
(c.) Inhaling the allergen when cutting fish.
(d.) All of the above.
2. Which of the
following will not protect against human infestation with Anisakis simplex?
(a.) Deep-freezing at -20 degrees Celsius for more than 48 hours
(b.) Cooking at temperatures higher than 60 degrees Celsius for 10 minutes
(c.) Keeping sushi at fridge temperature until it is served
(d.) None of the above
3. Which of the
following is true?
(a.) All histamine-sensitive individuals will react to the normal level
of histamine that is normally found in foods
(b.) No histamine-sensitive individual will react to a histamine dose
of lower than 50mg histamine/100g fish
(c.) Some histamine-sensitive individuals may react to only large doses
(d.) None of the above
4. Which of the
following does not have an effect on the level of histamine that affects
a sensitive individual?
(c.) Drugs such as dihydralazine, isoniazid, clavulanic acid, promethazine,
verapamil and metoclopramide
5. Which of the
following fish are truly responsible for inducing keriorrhoea?
(a.) Escolar, oilfish and rudderfish
(b.) Escolar and oilfish
(c.) Escolar and rudderfish
(d.) Oilfish and rudderfish
6. To what in the
flesh of the fish can kerriorrhoea be attributed?
(a.) The high levels of oil content
(b.) The indigestible wax ester content
(c.) The fact that the oil in the fish mainly comprises diacylglyceryl
ether or hydrocarbon
(d.) The presence of parasites
7. True or false:
The main feature of Ciguetera poisoning in humans is acute nephrotic
8. For what reason
is the intake of shark, marlin, swordfish and tuna restricted in pregnant
women, women of childbearing age and young children specifically?
(a.) Histamine content
(b.) The risk of Ciguetera poisoning
(c.) Methyl mercury content
(d.) Iodine content
|1. a [ ] b [ ] c [ ] d
||2. a [ ] b [ ] c [X] d
||3. a [ ] b [ ] c [X] d
|4. a [ ] b [X] c [ ] d
||5. a [ ] b [X] c [ ] d
||6. a [ ] b [X] c [ ] d
|7. a [ ] b [X]
||8. a [ ] b [ ] c [X] d
1. d. All of the
2. c. Keeping sushi at fridge temperature until it is served.
3. c. Some histamine-sensitive individuals may react to only large doses
4. b. Age
5. b. Escolar and oilfish
6. b. The indigestible wax ester content
7. b. False
8. c. Methyl mercury content