Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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marine oils have been related to prevention of heart

disease is noteworthy in modern Western societies

conscious of their health, and the consumption of

seafood is increasing significantly. (See Fish Oils:

Dietary Importance; Shellfish: Commercially Import-

ant Crustacea; Commercially Important Molluscs.)

0002 The majority of fish and shellfish are safe as food,

but there are some species that are naturally toxic

or poisonous and may cause illness or even death if

they are consumed. This article reviews raw-fish

dishes of Japan (e.g., Fugu), nature and risks from

ciguatoxins, caviar and its production, and eels and

their uses.

Raw-fish Dishes of Japan

0003 Raw-fish dishes – sliced fish flesh called sashimi in

Japan – have been served with vinegar for more than

1000 years, but are now more popular eaten with soy

sauce and grated Japanese horse radish. Flesh from

freshly caught fish is in the majority, but frozen–

thawed flesh is often supplied to the dishes. Bluefin

tuna (Thunnus thynnus), sea bream (Pagrosomus

major), striped bonito (Sarda orientalis), yellowtail

(Seriola quinqueradiata), and flounder (Paralichthys

olivaceus) are the species mostly consumable in all

seasons, and tiger puffer (Fugu rubripes) is considered

a prize delicacy in winter. The flesh for the dishes

should be of top quality regarding color, flavor,

taste, and texture.

0004Freshly caught bluefin tuna and striped bonito are

normally subjected to deep freezing, at a temperature

as low as 45



C, at sea to prevent myoglobin, the

dominant pigment in fish muscle, from turning to

metmyoglobin, which is a cause of meat discolor-

ation. Thus, the thawed flesh of deep-frozen tuna

and bonito is suitable to be served as raw-fish dishes.

0005More than 100 species of puffer fishes (family

Tetrodontidae) are broadly distributed from temper-

ate to tropical waters, but only about 10 species have

been consumed as human food by a handful of coun-

tries, principally Japan. There are marked differences

in toxicity among species, some being virtually non-

toxic. Fresh flesh and some parts of the puffer fish

may be enjoyed as raw or cooked dishes if properly

prepared, but other parts, such as ovary and liver, are

extremely toxic (Table 1). Only licensees may prepare

and serve dishes of the puffer fish for consumers,

under conditions specified by the Ministry of Health

and Welfare, because the major cause of food-

poisoning deaths is ingestion of toxic puffer fishes.

0006The responsible toxins are tetrodotoxin (TTX) and

related compounds (Figure 1). The lethal dose of TTX

for people is estimated to be 10 000 mouse units,

equivalent to 2 mg of TTX. Poisoning as a result of

eating puffer fishes is serious, and causes neurological

symptoms: tingling in the lips and extremities, paraly-

sis, and death by respiratory arrest and cardiovascular

collapse. The cardiovascular effects account for the

relatively high lethal rate in puffer-fish intoxications.

tbl0001 Table 1 Toxicity of puffer fishes

Species Ovary Testes Liver Skin Intestine Muscle

Fugu niphobles AC ABA C

F. poecilonotum AB ABB C

F. v e r m i c u l a r e v e r m i c u l a r e AD ABB C

F. pardale AC ABB D

F. vermiculare porphyreum AD ABB D

F. ocellatus obscurum AD BBB D

F. chrysops BD BBC D

F. rubripes rubripes BD BDC D

F. xanthopterum BD BDC D

F. stictonotum BD BCD D

Lagocephalus laevigatus inermis DD BDD D

L. lunaris spadiceus DD DDD D

Liosaccus cutaneus DD DDD D

Canthigaster rivulata DN CBC D

Diodon holacanthus DN DDD D

Chilomycterus affinis DN DDD D

Ostracion immaculatum DD DDD D

Lactoria diaphana DD DDD D

Aracana aculeata DD DDD D

A, strongly toxic, lethal at less than 10 g; B, moderately toxic, not lethal at less than 10 g; C, weakly toxic, not lethal at less than 100 g; D, negative, not

lethal at less than 1000 g; N, no data available.

Data from Hashimoto Y (1987) Marine Toxins and other Bioactive Marine Metabolites. Tokyo: Japan Scientific Societies Press.

2458 FISH/Miscellaneous Fish Products

0007 TTX has been demonstrated to be produced by

intestinal bacteria of TTX-bearing animals, as well

as some species of marine bacteria. This fact, along

with the distribution of TTX in nature, made it

possible to suggest the mechanism involved in the

toxification of TTX-bearers (Figure 2).

0008Nontoxic or slightly toxic puffer fishes have been

successfully cultured, and an increase in demand is

likely.

Nature and Risks from Ciguatoxins

0009About 300 species of fish and shellfish, inhabiting

shallow waters around coral reefs, have been known

to cause ciguatera, a poisoning with unique symp-

toms. Fish apparently become toxic and lose the tox-

icity rather more slowly. Although the name ciguatera

is derived from the Spanish term for a marine snail,

the syndrome is currently recognized as the result of

consumption of certain tropical fish. The risk of

ciguatera is highest from the consumption of herbiv-

orous reef fish or of the carnivorous fish that feed

on them.

0010It is thought that the principal source of ciguatoxin,

the most important toxin, is the benthic dinoflagellate

Gambierdiscus toxicus, which tends to cluster on the

surfaces of certain tropical seaweeds. Because of this

growth habit, the benthic dinoflagellate is efficiently

accumulated by herbivorous reef fish. Ciguatoxin

was isolated from G. toxicus obtained directly from

−

Tetrodotoxin

Tetrodonic acid

Anhydrotetrodotoxin

4-epi-Tetrodotoxin

HOH

COO

−

fig0001 Figure 1 Structures of tetrodotoxin and related compounds.

From Nakamura M and Yasumoto T (1985) Tetrodotoxin deriva-

tives in puffer fish. To x i c o lo g y 23: 271–276, with permission.

TTX-

producing

marine

bacteria

TTX

dissolved

in sea

water

TTX

absorbed

on and

precipitated

with

planktonic

carcass,

etc.

TTX

sediment

Flatworm

Ribbonworm

Arrowworm

Xanthid crab

Small

gastropods

Star

fish

Puffer fish

Tropical

goby

Large

gastropods

such as

trumpet

shell

(Parasitism

or symbiosis)

Vibro alginolyticus

V. damsela

Staphylococcus

Bacillus spp.

Pseudomonas spp., etc.

fig0002Figure 2 Assumed mechanism of toxification of TTX-bearing

animals. From Noguchi T, Arakawa O and Hashimoto K (1989)

Tetrodotoxin with special reference to its origin and the mechan-

isms involved in toxification of puffers. Journal of the Food Hygiene

Society (Japan) 30: 281–288, with permission.

FISH/Miscellaneous Fish Products 2459

coral reef seaweeds. Cultures of G. toxicus, however,

have been found to produce primarily a different

toxin, maitotoxin, the structure of which is not yet

clarified. Other benthic dinoflagellates, with growth

habits and distributions similar to those of G. toxicus,

may also be involved. The known differences between

ciguatoxin and brevetoxin lie in the longer duration

of the effects of ciguatoxin in human victims. Symp-

toms are nausea and neurological deficits similar to

those of paralytic shellfish poisoning, but more severe

and enduring. Victims of ciguatera occasionally com-

plain of relapses, in some cases precipitated by con-

sumption of alcohol, for months or even years after

the initial attack. Deaths are rare. The neurological

dysfunction includes a reversal of the sensations of

hot and cold, called ‘dry-ice’ sensation. The distribu-

tion of ciguateric fish cannot be defined strictly, but

distinct zones of toxicity are known by local fisher-

men. In notorious carnivorous fish, such as barra-

cuda, which are capable of both migrating and

accumulating high levels of toxin, it would be diffi-

cult to discriminate toxic fish from others.

0011 Although the characterization of ciguatoxin has

been a long-standing matter owing to the complexity

of the molecule and the difficulty in obtaining ad-

equate material, instrumental analyses with purified

material have elucidated the complete structure

(Figure 3). Chromatographic evidence indicates that

several other related toxins are also involved in cigua-

tera poisoning.

Caviar and its Production

0012 The eggs of many fish species, and of some other

aquatic animals such as sea urchin, are sought as a

food item. Caviar is one of the most well-known

names, especially in connection with sturgeon (Aci-

penser medirostris) eggs. Caviar and other fish egg

products are considered a specialty food and thus

tend to bring a high price.

0013Fish eggs have a substantial food value. On a

dry-weight basis, eggs contain 45–48% protein,

11–32% lipid, and 1.3–4.5% ash, respectively. To

produce caviar, live mature fish have to be used;

from dead sturgeon, it is difficult to remove the

eggs as they adhere firmly to the ovary sac. The

belly is cut open, from the pectoral fins to the anus.

The ovary is then drawn out and processed

immediately. The general procedure used in caviar

processing begins with washing the ovaries to remove

most of the blood and slime. The ovaries are then

cut open to extract the eggs. The egg-membrane

tissue of the sturgeon is normally hyperplasic and

muscular, but it can be softened enzymatically by

the action of lysozyme. The eggs are typically

salted, using either dry salting or a salt brining. For

dry salting, 10% (w/w) of salt is added to the

eggs as they are passed through a 33-mm sieve; stir-

ring may ensure faster and more effective penetration

of the salt into the eggs. After 3 h of salting, the

eggs are drained on a wire net. In the case of salt

brining, the eggs are allowed to stand for 1 h in

saturated brine, then drained upon a wire net over-

night. For further dehydration, the salted eggs

are pressed in a cotton bag. The salt-cured eggs are

packed in a container, tightly sealed, and stored at



C for aging.

0014Salted salmon eggs are called red caviar. The qual-

ity of red caviar depends on species, maturity, and

freshness of the eggs. The eggs should be of spawning

HHH

fig0003 Figure 3 Structure of ciguatoxin. From Murata M, Legrand AM, Ishibashi Y and Yasumoto T (1989) Structure of ciguatoxin and its

congener. Journal of the American Chemistry Society 111: 8929–8931, with permission.

2460 FISH/Miscellaneous Fish Products

salmon caught from coastal waters and be extracted

within 2 h of catching. Egg-membrane tissue in a

mature ovary is naturally hyperplasic and muscular,

and results in a low-quality product. It is also inad-

equate if eggs are used from the salmon late in the

fishing season, or immediately before spawning. A

high-quality red caviar is attributed to the use of

eggs of pink salmon (Oncorhynchus masou).

0015 Once separated from the raw salmon, the ovaries

are washed thoroughly in fresh water to remove

blood vessels and slime, then rubbed through a

gauze cotton net to isolate the eggs. An apparatus

consisting of gauze cotton net, a sloping wire net,

and a receiver is useful for commercial purposes.

The eggs that have been separated through the

gauze cotton net run down the slope and fall into

the receiver. The mass accumulated in the receiver is

put into a tub containing saturated salt brine (which

has been boiled and cooled prior to use), stirred for

20 min, removed and put into a basket, drained for

24 h, packed in a barrel or a wooden box, and cold-

stored for aging.

0016 The oil content of salmon eggs averages 12% on

the basis of total weight. Salmon eggs yield a light-

colored oil. The oil contains about 45% of highly

unsaturated fatty acids with molecules having 20–22

carbon atoms. About one-third of the total fat is

phospholipid, probably lecithin. The protein of

salmon eggs is of a high quality. It contains all of the

eight essential amino acids (isoleucine, leucine, lysine,

methionine, phenylalanine, threonine, tryptophan,

and valine) in substantial amounts. Salmon egg

protein is relatively high in lysine, methionine, and

isoleucine. (See Amino Acids: Metabolism.)

Eels and their Uses

0017 Eels are difficult to sell in the USA but are highly

prized in Europe and several areas of the Far East,

including Japan. The major species of food eels are

freshwater eels (Anguillidae), pike eels (Muraensoci-

dae) and conger eels (Congridae). Of the 16 species of

Anguilla eels found worldwide, most are in the waters

around Southeast Asia. Anguilla japonica and A. mar-

morata are the inhabitants in the waters around

Japan, while A. rostrata and A. anguilla are in

the Atlantic. For food eels, the important species are

A. japonica and A. anguilla. Muraenesox cinereus is

the commercially valuable species of pike eel. Conger

eels number about 110 species in the world, but

white-spotted conger (Conger myriaster) is the only

species prized as food. Eels are mostly processed to

produce ‘spitchcock’ with seasoning juice. Eels

weighing roughly 200 g are put into a basket and

subjected to cut-feed for a couple of days in running

water. In producing ‘spitchcock,’ back-cutting, meat

separating, and sizing are the initial processes, per-

formed manually. The spiting and broiling processes

are carried out mostly by machines.

0018In the broiling process, an infrared ray burner is

commonly used. The broiling time depends on the

flame temperature and the size of the slices of flesh,

but generally, 4–5 min is long enough for the first

broiling without seasoning juice, then 5–10 min for

the second broiling with the juice. A seasoning juice is

brushed over the flesh surface during an automated

run from the first to the second broiling processes.

The broiling process greatly affects the food quality:

either insufficient or excessive broiling gives a bitter

or burnt flavor to the product. The seasoning juice

consists of soy sauce, sugar, and sweet liquor, in a

ratio of 1:1:0.5.

0019Smoked eel is another type, traditionally popular

in Europe, and is widely consumed. Preliminaries for

processing smoked eels are almost similar to those for

‘spitchcock.’ The fresh fillets are cured in 5–10% salt

brine for about 10 h; salt concentration and curing

time are controlled according to the size of the fillet.

The cured fillets are then subjected to trimming,

washing, draining, and drying. Smoke drying is im-

portant in processing smoked eel and is performed at

a controlled temperature within 60–80



C for 5–6h,

using hardwood or sawdust. A gradual increase in

temperature, using adequate amounts of sawdust,

is required to prevent the flesh from scorching.

The half-finished product is taken out from the

smoking kiln, any soot is swept off, and the fillets

are arranged in a carton box to equalize the water

contents.

0020The ‘spitchcock’ eels are the traditional food of

Japanese people during the hottest period of the

summer. They contain (per 100 g of eel) 47.1 g of

water, 23.0 g of protein, 24.4 g of lipid, 3.1 g of non-

fibrous carbohydrate, 2.4 g of ash, 150 mg of calcium,

300 mg of phosphorus, 0.8 mg of iron, 510 mg of

sodium, 300 mg of potassium, 150 mg of retinol,

5000 IU of retinol potency, 0.75 mg of thiamin,

0.74 mg of riboflavin, and 4.1 mg of niacin. Refer to

individual nutrients.

0021Pike eel is a white-flesh fish, which is rich in fat and

taste, and consumable as ‘spitchcock,’ soup, or

‘vinegared’ products, or, after processing, to surimi

(ground meat), as the base for a high-quality fish-gel

product. However, a number of tiny bones remaining

in the flesh are disadvantageous in processing any

type of marine food.

See also: Amino Acids: Metabolism; Fish Oils: Dietary

Importance; Shellfish: Commercially Important

Crustacea; Commercially Important Molluscs

FISH/Miscellaneous Fish Products 2461

Further Reading

Hall S (1991) Natural toxins. In: Word DR and Hack-

ney CR (eds) Microbiology of Marine Food Products,

pp. 301–330. New York: Van Nostrand Reinhold.

Motohiro T (1975) An elementary knowledge of frozen

food. In: Amano K, Kaneko S, Kameda K et al. (eds)

Handbook of Frozen Food, pp. 39–42. Tokyo: Asakura-

Shoten.

Tanikawa E, Motohiro T and Akiba M (1985) Marine

Products in Japan, 2nd edn. Tokyo: Koseisha Koseikaku.

Spoilage of Seafood

P Dalgaard, Technical University of Denmark, Lyngby,

Denmark

Background

0001 The world’s annual production in capture fisheries

has remained at * 90 million tonnes during the last

decade, and only aquaculture production in marine

and fresh water has allowed for global increases in

raw material for fishery products. At the same time,

international trade in seafood is increasing, and opti-

mal utilization of available resources and prevention

of losses during storage and distribution are more

important than ever. Most seafoods have a short

and variable shelf-life, and the increasing interest in

marketing of less preserved products makes preven-

tion of spoilage an important challenge.

0002 The flesh of most fresh fishes has a high pH of 6–7

post rigor and a high content of free amino acids in

the muscle extractives. Many marine and some fresh-

water species contain trimethylamine oxide (TMAO),

resulting in a high muscle redox potential, and some

species contain high levels of polyunsaturated fatty

acids. Furthermore, fish and shellfish often harbor a

natural psychrotolerant microflora. These specific

properties result in microbial activity and lipid oxida-

tion being responsible for spoilage of most fresh and

lightly preserved products. This explains the short

shelf-life of these products (Table 1). Postharvest

losses of food have been estimated to be as high as

* 25% resulting from microbial activity alone, and

this problem is particularly relevant for seafood. To

reduce losses resulting from spoilage and to insure

that products are safe at the time of consumption,

knowledge about product shelf-life under different

storage conditions is important. Storage temperature,

packaging, hygienic standard of raw material, and

gutting are the most important factors influencing

the shelf-life of seafoods (Table 1).

0003When new seafoods are developed, or existing prod-

ucts are modified or stored under new conditions,

shelf-life must be determined by sensory methods.

However, product attributes, to be measured by

instrumental methods, are useful when industry and

national or international authorities need to evaluate

raw material or products. Development of such instru-

mental methods and techniques to predict shelf-life

can rely on information about reactions responsible

for product spoilage. The present article concerns

these microbial, chemical, and biochemical spoilage

reactions and methods to determine and predict shelf-

life of seafood. In addition, safety hazards related to

seafood consumption are presented.

Sensory Changes and Shelf-life

0004Sensory properties of seafood, as determined by the

senses of sight, smell, taste, and touch change during

storage, and a series of phases can be identified in

most products. Fresh fishes typically have a species-

specific taste and odor that disappear after a few days

of chilled storage. Later, off-odors and off-tastes, i.e.,

off-flavors, which are often ammonia-like, fishy, sour,

sulfurous, or yeasty become notable, increasing in

intensity and finally resulting in overt spoilage. Sens-

ory methods relying on panels of trained assessors are

used to determine the shelf-lives of products based on

the degree of sensory changes.

0005Sensory methods frequently used with seafoods

include the Torry scheme, various simplifications of

this method, EU schemes for freshness grading, and

the quality index method (QIM). The Torry scheme,

developed in Scotland in 1948 for fresh fishes, relies

on the assessment of raw appearance, raw odor, raw

texture, cooked odor, cooked texture, and cooked

flavor of samples. Each quality attribute is scaled by

five or 10 descriptive terms. Numerous less extensive

sensory schemes have been used to determine the

shelf-life from the appearance, odor, taste, and

texture of raw or cooked products. Often, sensory

changes are expressed as a simple overall grading

(I, II, or III) and shelf-life determined as the time

when the percentage of samples in grade III reaches

a defined level. The EU requires numerous fish and

shell-fish to be graded by specific EU schemes if

marketed within the community. Assessments of ap-

pearance, odor of skin, outer slime, eyes, gills, and

peritoneum are carried out with whole or gutted fish.

Assessments are typically carried out in auctions by

trained personnel, and fish are placed into grades

Extra (E), A, B or Unfit (C), based on schemes for

2462 FISH/Spoilage of Seafood

different groups of species. These freshness categories

do not allow the remaining product shelf-life to be

determined directly, and the demerit point or QIM

can be used to obtain this information. The QIM

relies on sequential evaluation of a relatively large

number of fish attributes. Demerit or QIM points of

a sample, i.e., the sum of the attribute scores, increase

linearly with product storage time, and rates of spoil-

age at a constant storage condition can be calculated

easily. QIM schemes allow the remaining shelf-life of

whole or gutted fish of several species to be deter-

mined. Evaluation of fish fillets remains difficult,

and further studies are needed to validate QIM

for determination and prediction of the shelf-life of

fresh fish above 0–5



C, i.e., when products are

temperature-abused.

Microbiological, Chemical, and

Biochemical Changes

0006 Sensory methods are always needed to determine the

shelf-life of new or modified seafoods. Unfortunately,

sensory methods relying on a panel of assessors

are expensive to use and difficult to calibrate. There-

fore, it is desirable to supplement or replace sensory

evaluations by instrumental analyses. Instrumental

methods are important, e.g., to determine whether

the characteristics of seafoods comply with speci-

fications as part of purchase agreements or with

standards and guidelines established by national or

international authorities.

0007Microbial activity is responsible for spoilage of

most lean fresh and lightly preserved seafood. Chem-

ical reactions, primarily oxidation and activity of

autolytic enzymes, become important spoilage reac-

tions when microbial activity is reduced by processing

or preservation (Table 2). It is noteworthy that

the range of product characteristics and storage con-

ditions within which a particular spoilage reaction

actually limits product shelf-life remain poorly de-

scribed for practically all seafoods.

Microbiological Changes

0008Fish and shellfish are poikilotherms, i.e., their body

temperature is similar to that of their surroundings,

tbl0001 Table 1 Shelf-life of selected seafoods

Product Storage temperature (



C) Packaging Shelf-life (days)

Fresh seafood

White-fleshed from temperate/cold waters 0 Air or VP 12–18

Cod 2.5 MAP 36

Caught in warm waters 0 Air 18–35

Tilapia 4 MAP > 25

Large fishes like halibut, tuna, and salmon 0 Air or VP 19–22

Dark-fleshed, small fish

Low-fat 0 Air 6–9

High-fat 0 Air 4–6

Shellfish, temperate and cold waters 0 Air 3–10

Shellfish, warm waters 0 Air 8–12

Sharks and rays 0 Air 8–10

Frozen and thawed 0 Air 12–18

Thawed cod 2 Air or VP 9–12

Thawed cod 2 MAP 12–>20

Sous vide cooked 3–4 VP 15–>21

Lightly preserved

Cold-smoked salmon 5 Air * 14

Cold-smoked salmon 5 VP 20–56

Hot smoked cod (lightly salted) 0–1 Air 24–26

Brined roe (lump fish) 5 VP 75–90

Cooked and brined shrimps 5 Air 40–>60

Cooked and brined shrimps 5 MAP 84–>200

Semipreserved and preserved

Cod (salted) 0 Air 500

Sugar salted herring 5 Brine > 360

Frozen

Whitefish, whole or fillet blocks 18 Glazed 120–240

Fatty fish 18 Glazed 90–120

Mackerel 26 VP > 540

MAP, modified-atmosphere-packaging; VP, vacuum-packaging.

Modified from Dalgaard P (2000) Fresh and lightly preserved seafood. In: Man CMD and Jones AA (eds) Shelf Life Evaluation of Foods, 2nd edn.

pp. 110–139. Gaithersburg, MD: Aspen.

FISH/Spoilage of Seafood 2463

tbl0002 Table 2 Seafood spoilage indicators

Spoilage indicator Sensory property Spoilagereaction Examples of productswhere compounds are formed

Trimethylamine (TMA) Ammonia-like Microbial Most marine fishes and in some fresh water fishes like Nile perch

and tilapia that contain TMAO

Ammonia Ammonia Microbial and enzymatic Particularly in cephalopods, crustaceans, and dark-fleshed fishes

HistaminePepper-like

MicrobialTuna,mackerel,mahi-mahi,herring,anchoviesandotherseafoods

withahighleveloffreehistidine,particularlywhenstored>5



Cadaverine, putrescine, and tyramine Putrid, rotten

Microbial Most fresh and lightly preserved seafoods

Volatile sulfur compounds Sulphurous, rotten Microbial Aerobically stored fresh fish, temperature-abused fresh and lightly

preserved products, but also sporadically in sous vide cooked and

chilled fish where very high levels can be observed

Short-chain alcohols and carbonyls (ethanol,

propanol, butanol, 2-methylbutanal,

3-methylbutanal, 2,3-butadione)

Solvent-like, malty Microbial Most fresh and lightly preserved seafood

Hypoxanthine (Hx) Bitter taste Enzymatic and microbial All fishes, but rates of Hx formation vary markedly between species

owing to differences in activity of the autolytic enzymes that

generate the substrate precursor inosine. As examples, Hx

formation is very rapid in redfish, modest in cod, slow in mackerel,

and very slow in swordfish

Dimethylamine (DMA) Ammonia-like Enzymatic TMAO containing seafood and particularly in hake when stored

frozen at >20



Free fatty acids (C

–C

) Rancid, oily, bitter and metallic Enzymatic Fatty fishes stored at conditions of temperature abuse as well as in

both lean and fatty fishes during frozen storage at inappropriately

high frozen storage temperatures

Propanal Solvent-like Chemical From oxidation of n-3 fatty acids

Pentane, hexanal Chemical From oxidation of linoleic acid and useful at indicator for this type of

oxidation

Cis-4-Heptanal Cardboardy, paint-like Chemical During frozen storage of cod

2,4-Heptadienal, Stale, whale oil flavor Chemical Fatty fishes and fish oil containing products

2,4,7-Decatrienal

As a result of high flavor detection thresholds, biogenic amines contribute to the spoilage of seafood only when present in extremely high concentrations.

and the often complex microflora on their outer sur-

faces to some extent reflect the microbiology of the

water in which they live. However, only some of

the numerous species of microorganisms on live fishes

are important in seafood spoilage. In fact, a pattern of

microbial growth and activity during storage of sea-

food is frequently observed; the so-called specific

spoilage organism (SSO) concept (Figure 1). On

newly processed, fresh, or lightly preserved seafood,

the SSOs are usually present in very low concentra-

tions and constitute only a minor part of the total

microflora. During storage under particular condi-

tions of temperature, atmospheres, NaCl, available

water, preservatives, etc., SSOs, which are often a

single microbiological species, grow faster than the

remaining microflora, produce metabolites respon-

sible for off-flavors, and finally cause sensory rejec-

tion of a product (Figure 1). SSO are typically present

at levels of about 10

colony-forming units (cfu) g

1

when products become sensorily spoiled. In contrast

to SSOs, the spoilage microflora, i.e., the microflora

found at the time of sensory product rejection,

are frequently a mixture of microbial species, some

of which can be unimportant in terms of spoilage.

The substantial importance of microbial activity in

seafood spoilage has been established by comparing

off-flavor development in sterile and naturally con-

taminated blocks of fish muscle. Identification of a

SSO relies on a comparison of product spoilage char-

acteristics with those of isolates from the spoilage

microflora. Spoilage potential and spoilage activity

are evaluated as the qualitative and quantitative abil-

ity, respectively, of isolates to produce off-odors and

spoilage metabolites. The yield factor for production

of a metabolite by a microorganism is a measure of

the amount of metabolite produced per cell. Yield

factors are most useful to determine whether the

levels of cells and metabolites in a seafood correspond

to the spoilage activity of an isolate from the spoilage

microflora, i.e., if the isolate is likely to be the SSO.

Evaluation of proteolytic activity need not be in-

cluded in SSO identification, because microorganisms

metabolize seafood extracts, primarily free amino

acids and TMAO, and causes sensory product spoil-

age before protein degradation is detected.

0009As shown in Figure 1, the level of SSO and their

metabolites can be used as indices of product spoil-

age. Furthermore, product shelf-life can be predicted

from the initial level and from the growth rate of

an SSO. Finally, it follows from the SSO concept

that targeted inhibition of a SSO can be used in the

development of new products that have an extended

shelf-life.

0010The SSOs of a number of seafoods have been iden-

tified and habitats of the live fishes, product charac-

teristics, and storage conditions clearly determined

the microorganisms responsible for product spoilage

(Table 3). The specific parameters that allow certain

microbial species to become dominant in the spoilage

microflora can be determined by studying SSOs in

pure cultures. As an example, Shewaenella putrefa-

ciens-like bacteria grow vigorously at the pH of most

fresh seafoods but are substantially inhibited at pH

values below 6. This explains why Pseudomonas spp.

are more important SSOs in aerobically stored fresh

seafoods with a pH of * 6 or below. S. putrefaciens-

like organisms, P. phosphoreum, Aeromonas spp.,

species of Enterobacteriaceae and Vibrio spp. reduce

TMAO to trimethylamine (TMA) in anaerobic respir-

ation. This facilitates their growth in vacuum or

modified-atmosphere-packed seafoods and explains

the development of TMA in different fresh and lightly

preserved packed products. Spoilage of these prod-

ucts, however, can also be caused by lactic acid bac-

teria, although these are unable to reduce TMAO to

TMA. Gram-positive microorganisms are generally

more resistant to heat, frozen storage, salt, low

water activity, low pH, high carbon dioxide levels,

and irradiation than Gram-negative microorganisms.

However, existing data for the quantitative effect of

environmental parameters on growth kinetics of

microorganisms are insufficient to predict precisely

the microbial species that become the SSO in a sea-

food, where combinations of product characteristics

or storage conditions have not previously been evalu-

ated in storage trials with naturally contaminated

products.

0011Shewanella putrefaciens-like organisms are primar-

ily important in spoilage of aerobically stored fresh

fish (Table 3) but they also may contribute to spoilage

Storage time

Shelf life

Chemical

spoilage

index

Minimal

spoilage

level

TVC

SSO

Metabolites

Log (cfu/g)

Conc. of metabolites

fig0001 Figure 1 Specific spoilage organism (SSO) concept. Typical

changes in total viable counts (TVC), SSO, and metabolites pro-

duced by SSO during storage of fresh seafood. Modified from

Dalgaard P (2000) Fresh and lightly preserved seafood. In: Man

CMD and Jones AA (eds) Shelf Life Evaluation of Foods, 2nd edn,

pp. 110–139. Gaithersburg, MD: Aspen with permission.

FISH/Spoilage of Seafood 2465

of vacuum-packed seafoods if present in high levels

when products are packed. P. phosphoreum is primar-

ily important in spoilage of packed seafood (Table 3),

but it produces TMA in some aerobically stored fresh

fish, and it remains unclear as to what extent this

contributes to spoilage of the aerobically stored prod-

ucts. High levels of Aeromonas spp., with a substan-

tial spoilage potential, have been detected in both

chilled and temperature abused freshwater fish stored

aerobically or under modified atmosphere packaging.

The importance of these organisms in spoilage needs

further study, as do the taxonomy and metabolism

of the Vibrio spp. and species of Enterobacteriaceae

occurring in temperature-abused seafoods (Table 3).

Psychrobacter immobilis is frequently observed in

high concentrations in seafood but is not included as

a SSO in Table 3, because of a very limited spoilage

potential. Recent studies suggest that lipolytic activity

of these organisms contributes to the spoilage of fresh

sardines, and this deserves further investigation.

Finally, it should be stressed that, for numerous sea-

foods, the SSOs and their spoilage domain, i.e., the

range of product characteristics and storage condi-

tions within which a particular SSO causes spoilage,

remain to be identified. This is particularly the case

for lightly preserved products processed by various

emerging preservation technologies and products

containing seafood together with other ingredients.

Chemical and Biochemical Changes

0012 Chemical, biochemical, and other changes in seafood

are frequently studied with the objective of identify-

ing indices of freshness or spoilage to be measured

by instrumental methods in relation to processing or

distribution. Single compound quality indices (SCQI)

have been studied to find an individual substance for

which the concentration increased during storage to a

critical level corresponding to sensory product rejec-

tion. Owing to the complex and dynamic nature of

seafood spoilage, SCQI often have a limited range of

applicability with respect to product characteristics

and storage conditions. Consequently, sums or ratios

of concentrations of several compounds have been

used as indices of freshness or spoilage. More recently,

multiple compound quality indices (MCQI) have been

developed using multivariate statistical methods

to select a combination of instrumentally measured

responses that correlate with changes in sensory attri-

butes or remaining shelf-lives of products.

0013Total volatile nitrogen (TVN) and TMA are im-

portant indices of spoilage in fresh and lightly pre-

served seafood. TVN primarily includes ammonia,

TMA, and DMA. The European Commission (Coun-

cil Regulation No. 95/149/EEC) specified that TVN

should be used as an index of spoilage when sensory

evaluation casts doubt on fish freshness. Critical

limits of 25–35 mg-N of TVN per 100 g have been

indicated for different fish species. In TMAO-

containing seafood, 10–40 mg-N of TMA per 100 g

are typically present at the time of sensory spoilage.

Nevertheless, Pseudomonas spp. can spoil, e.g., fresh

Nile Perch without transforming its content of TMAO

into TMA. Off-flavors caused by volatile amines

depend on pH and possibly other product character-

istics. Sugar-salted herring with a pH of < 6, for

example, may contain as much as * 75 mg-N of

tbl0003 Table 3 Specific spoilage organisms in seafood

Seafoods Typical specificspoilage organism

Fresh and chilled, stored in air Shewanella putrefaciens-like

a,b

Pseudomonas spp.

Fresh, chilled and stored in vacuum or modified-

atmosphere packaging

Photobacterium phosphoreum

Lactic acid bacteria

Brochothrix thermosphacta

Fresh and lightly preserved products stored at

ambient temperature

Aeromonas spp.

Vibrio spp.

Enterobacteriaceae

Enterococcus faecalis

Sous-vide cooked and chill stored Gram-positive spore formers

Lightly preserved

and chill-stored Lactic acid bacteria

Enterobacteriaceae

P.phosphoreum and other marine Vibrio spp.

Semipreserved, salt cured and chilled Halobacterium spp., Halococcus spp. and osmotolerant molds and yeasts

Fermented and chilled Molds and lactic acid bacteria

Refer to Shewanella putrefaciens, Shewanella baltica, and other closely related H

S-producing, Gram-negative bacteria.

Typical of fishes from marine and temperate waters.

Typical of fishes from freshwater and fishes from warmer waters.

Include, for example, cold-smoked salmon, cooked and brined shrimps and brined roe products.

Include, for example, Lactobacillus curvatus and Lactobacillus sake.

2466 FISH/Spoilage of Seafood

TVN per 100 g and * 35 mg-N of TMA per 100 g

without appearing sensorially spoiled. Even in

TMAO-containing seafood, little TMA is produced

until the SSO reaches high numbers and TMA

can only be used as an index of spoilage and not

as an index of freshness (Figure 1). Gadoid fishes

and maybe some other species contain the enzyme

TMAOase (EC 4.1.2.32) in their muscle tissue.

The enzyme transforms TMAO into DMA and

formaldehyde. The later causes protein denaturation

and textural changes in fish muscle tissue, and the

DMA content correlates with the sensory texture

ratings of thawed hake. TMAOase is most active at

5to10



C, but in hake, substantial amounts of

DMA can be formed during frozen storage above

20



C. In contrast with white-fleshed fish, consider-

able amounts of ammonia can develop in cephalo-

pods, crustaceans, and dark-fleshed fish like herring,

owing to their high content of free amino acids.

Clearly, the usefulness of TVN, TMA, and DMA as

indices of spoilage depends strongly on the fish

species and storage conditions.

0014 In chilled fresh and lightly preserved seafood,

adenosine triphosphate (ATP) is degraded sequen-

tially into adenosine diphosphate (ADP), adenosine

monophosphate (AMP), inosine monophosphate

(IMP), inosine (Ino), and hypoxanthine (Hx). IMP is

formed by autolytic enzymes, whereas spoilage bac-

teria contribute to Ino and particularly Hx formation.

The K-value ¼([Ino] þ[Hx]) 100/([ATP] þ[ADP]

þ[AMP] þ[IMP] þ[Ino] þ[Hx]) and the quantita-

tively similar K

-value ¼([Ino] þ[Hx]) 100/([IMP]

þ[Ino] þ[Hx]) and G-value ¼([Ino] þ[Hx]) 100/

([AMP] þ[IMP] þ[Ino]) are used as measures of fish

freshness. In Japan, the critical K-value limit for fish

to be consumed raw is 20. These values increase

linearly during the first days of chilled storage of

most fishes and therefore can be used as indices of

freshness. However, in some fish species, e.g., redfish,

the K-value reaches maximal levels well before sens-

ory rejection and cannot be used as a general index of

spoilage (Table 2).

0015 Production of biogenic amines in seafood varies

strongly owing to large variations in the free amino

acid precursors between fish species and the variabil-

ity in the ability of spoilage bacteria to produce agma-

tine, cadaverine, histamine, putrescine, spermidine,

spermine, tyramine, and tryptamine. Consequently,

individual biogenic amines are rarely appropriate as

SCQI. However, different ratios or sums of concen-

trations of biogenic amines as well as dedicated

MCQI have been suggested and critical limits cor-

responding to the end of shelf-life determined, e.g.,

for fresh salmon, herring, lobster tails, mahi-mahi,

plaice, rockfish, shrimps, tuna, whiting, and cold-

smoked salmon. Biogenic amines are heat-stable and

therefore, together with organic acids, appropriate

for evaluation of raw material used in canned

products. The effect of temperature, NaCl, pH, and

atmosphere on microbial formation of biogenic

amines in seafood needs further study.

0016The activity of spoilage microorganisms frequently

results in the formation of volatile sulfur compounds,

short-chain organic acids, aldehydes, ketones, and

alcohols, and some of these metabolites are clear

indices of spoilage owing to their very unpleasant

odors. However, critical concentrations correspond-

ing to the end of shelf-life remain to be determined

and validated.

0017Degradation of lipids by enzymatic hydrolysis or

chemical oxidation can result in rancid off-flavors in

seafood. In chilled but particularly in temperature-

abused fresh fatty fish, enzymes from tissue, intestinal

content, and possibly microorganisms hydrolyze tri-

acylglycerol into free fatty acids, causing the so-called

acid rancidity. Free fatty acids are also formed by

enzymatic hydrolysis during frozen storage of both

lean and fatty fishes. With salmon, frozen storage

of raw and cooked samples confirmed enzymatic hy-

drolysis as being responsible for the formation of free

polyunsaturated fatty acid. Aroma-recombination

studies with fresh fish showed these acids to cause

the same oily, bitter, and metallic taste as observed

after frozen storage of salmon. Lipid oxidation limits

the shelf-life of several frozen and dried seafoods as

well as of fish oil-containing products. The peroxide

value (PV) and the thiobarbituric acid reactive sub-

stance (TBARS) value are classic measures of primary

and secondary oxidation products, respectively. Pri-

mary oxidation products have no off-flavor and may

be both formed and degraded during storage of sea-

foods. However, seafoods with PV of 10–20 meq of

peroxide per kilogram of lipid and TBARS values

of 1–2 mmol of malonaldehyde equivalents per gram

of product fat often have rancid off-flavors.

0018It is laborious to identify microbial metabolites,

oxidation products, or other compounds to be used

as indices of spoilage. Chromatographic (gas chroma-

tography and high-performance liquid chromatog-

raphy) and spectroscopic techniques including near

infrared and nuclear magnetic resonance can be used

to determine various changes in seafoods during stor-

age. Chromatographic and spectroscopic techniques

provide large amounts of data, and in order to extract

compounds or responses that correlate with sensory

changes, multivariate statistical methods, particularly

partial least-squares regression, can be applied.

Identified combinations of compounds or responses

can be used as MCQI, and the approach may facili-

tate development of methods for rapid detection of

FISH/Spoilage of Seafood 2467