Recent advances in harvest and post-harvest technologies in fisheries

Microbial toxins in seafood

Anupama T. K.
Microbiology, Fermentation and Biotechnology Division
ICAR- Central Institute of Fisheries Technology, Cochin
[email protected]
Introduction
According to the Food and Agriculture Organization (FAO, 2020), global fish
production has reached to 179 million tonnes in 2018 with a total value of USD 401 billion.
Out of that, 156 million tonnes were used for direct human consumption and remaining 22
million tonnes for non-food uses. Global fish consumption has increased from 9.0 kg percapita
in 1961 to 20.5 kg in 2018, by about 1.5 percent every year. The fish consumption accounted
for 17 percent of total animal protein, and 7 percent of all proteins, consumed globally (FAO
2020). Live, fresh or chilled fish are the most preferred items and utilized maximum (44
percent) for direct human consumption. The rest of production is processed, with 35% frozen,
11% in prepared and preserved forms, and 10% cured (FAO, 2020). Seafood is one of the most
traded food commodities (USD 164 billion) in the world. Nearly, 75% of the seafood was
imported by the developed countries in international trade and 50% was exported by
developing nations.
Fish is considered as safe and healthy food for consumption. However, it is well known
those microorganisms are present on fish surface, skin, gills, digestive tract and internal organs.
Several outbreaks were reported in association with bacterial pathogens, biotoxins, histamine,
viruses, and/or parasites by the consumption of raw or undercooked fish and fish products
(Galaviz-Silva et al., 2009). Both pathogenic and spoilage bacteria can be added to fish at any
stage of transportation, handling, processing and storage. According to the U.S. Centers for
Disease Control and Prevention (CDC), fish was considered as food category commonly
implicated in food borne outbreaks involving single food categories (CDC, 2018). A total of
937 food borne outbreaks associated with fish were reported, resulting in 5,011 illnesses, 364
hospitalization, and four deaths in past ten years in United States (CDC, 2018). The fish and
fish products have been continuously implicated in food borne outbreaks, contributing 7% of
total confirmed food borne-illness outbreaks over recent years (CDC, 2018). The significant
increase in food borne outbreaks may be due to the rise of new nutritional trends which supports
the consumption of raw or fresh foods. According to CDC 2014, there are 31 major pathogens
are reported which can cause 32 diseases in human. The most common outbreaks associated
with consumption of fish is scombroid toxin or histamine, Salmonella spp. and Clostridium
botulinum, Clostridium perfringens.
Bacterial Toxin
Food borne illness caused by the pathogenic bacteria is an important concern in
seafood. The most common types of food borne illness in human are infection and intoxication.
Food borne infections are caused by ingesting live pathogens that develop inside the body,
generally in the intestine tract. Intoxication is a condition caused by swallowing preformed
toxins i.e. toxins created by microorganisms in the food before it is consumed. Furthermore, a
toxic-infection (also known as toxin-mediated infections), is caused by the ingestion of
pathogens, which produce biologically active toxins in the small or large intestine. Both gram

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positive and gram negative bacteria can able to produce toxins. They can produce even single
or multiple toxins. Toxin production as a result of (excessive) microbial proliferation can occur
at any point in the food production chain. Even though the bacteria were killed during the food
processing steps, the toxin remains resident and biologically active. The toxin production in
food is influenced by extrinsic (e.g., temperature, humidity, atmosphere) and intrinsic (e.g.,
pH, aw, nutrients) properties , cell density, growth phase, cell stress, and injury .The ability of
toxins production in humans to cause disease symptoms depends on several factors including
strain pathogenicity, quality of toxin produced, physic-chemical characteristics of toxins,
interactions with food components, metabolites produced by microorganisms, stability in food
and in the human gastrointestinal tract, inherent (sub)clinical dose of toxins, mode of action,
effect of acute and (sub)chronic exposure, and targets and receptors in the human body
(Rajkovic et al., 2020).
Types of Toxins
A bacterial toxin is a protein-based macromolecule that can cause toxic harm to a
specific organ of the host (Iriarte et al., 2001). Toxins can be divided into endotoxins and
exotoxins:
Endotoxins: These are the components of Gram-negative bacteria's outer membrane; they are
the most important antigen of the bacteria, and they are released into the medium during various
processess such as lysis and cell division. This endotoxin can able to cause endotoxic shock
and tissue damage.
Exotoxins: These are protein-derived macromolecules that the bacterium produces and then
releases into the media. Depending on their mechanism of action, exotoxins are classified as
follows:
Toxins Type I: These toxins alter the cells of the host’s without internalizing in the cells;
for example, the superantigens produced by Staphylococcus aureus.
Toxins Type II: Within this group there are hemolysins and phospholipases; they cause pore
formation and/or membrane destruction in the host cells. The pathogen can penetrate the host
cell using this virulence factor. Eg: aerolysin and GCAT protein produced by Aeromonas spp.
Toxins Type III: These toxins are known as A/B due to their binary structure. Fraction B binds
to the receptor of the cell and fraction A has enzymatic activity, which, depending on the toxin
and its mechanism of action, will cause cell damage; for example, the Shiga toxin produced by
Escherichia coli O157:H7, the Cholera toxin (Ctx) produced by Vibrio cholerae, and the
Anthrax toxin produced by Bacillus anthracis
The exotoxins produced by bacteria play an important role in the pathogenesis of
diarrheal illness, inducing excessive liquid secretion without the destruction and death of
intestinal mucosal cells. These toxins are generically referred to as enterotoxins (Hernández-
Cortez et al., 2017)
Toxins produced by pathogens involved in foodborne diseases are as follows:
 Bacillus cereus,
 Clostridium botulinum,
 Clostridium perfringens and
 Staphylococcus aureus.
 Pathogenic Escherichia coli
 Vibrio cholera

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 Shigella spp.
 Yersinia enterocolitica
Bacillus cereus
Bacillus cereus is one among the Bacillus spp. that has been identified as the most
frequent cause of foodborne illness. B. cereus is commonly found in many raw and unprocessed
foods and the presence of low numbers of B. cereus in raw foods is regarded normal, while the
numbers more than 5 log CFU/g (or per mL) are considered as a hazard to food safety (Sanchez-
Chica, et al., 2020). B. cereus usually found in rice, pasta, dairy, meat and seafoods. Food
poisoning due to this organism may occur when foods are prepared and held without adequate
refrigeration for several hours before serving. The B. cereus spores can withstand heat
processes, and germinated vegetative cells can multiply and produce toxins under ideal
conditions. Therefore, in order to inactivate B. cereus, suitable time/temperature profile must
be developed, which will be often specific for specific foods as well as maintain cold chain due
to psychotropic character of some strains of B. cereus (Webb et al., 2019).
B. cereus toxins cause two distinctly different forms of food poisoning—the emetic or
vomiting type and the diarrheal type. The emetic type is an intoxication caused by the presence
of emetic toxin, cereulide, in food. Cereulide intoxication is characterized by the quick onset
of symptoms (0.5 to 6 hours), which include nausea, vomiting, and occasionally abdominal
cramps and/or diarrhoea, which normally resolve within 24 hours. The Intoxication/infection
dose is ca. 10 μg/kg−1 bw, 0.01μg/g1 of food (produced by B. cereus of more than 105 CFU/g
food, depending on the strain, food and condition. The diarrheal type is produced by the
synthesis and release of protein enterotoxins in the small intestine after consumption of viable
B. cereus vegetative cells and/or spores. Hemolysin BL (Hbl), nonhemolytic enterotoxin (Nhe),
and cytotoxin K are known to be implicated in this syndrome. They are all heat labile, pH
sensitive, and proteases sensitive proteins, which is why preformed toxins in food typically do
not result in foodborne intoxication (Rajkovic et al., 2020). The symptoms of diarrheal type
are characterized by the onset of watery diarrhea, abdominal cramps, and pain occurs 6-15
hours after consumption of contaminated food. Nausea may accompany diarrhea, but vomiting
rarely occurs. The heat toxin stability of diarrheal type is 5 min. at 56 ºC whereas emetic
type(cereulide): 90 min at 121 ◦C.
Control measures: Proper hygiene and appropriate temperature control should be
maintained throughout the production and storage. Optimization of heat process and
temperature control to prevent spore germination and multiplication of vegetative cells of B.
cereus, quick chilling methods to cool foods below 7.2º C within 4hrs of preparation should be
followed.
Clostridium botulinum
Clostridium botulinum is a dangerous food poisoning organism and it produce a very
deadly, exotoxin (neurotoxin) when grows in food. The food poisoning caused by this organism
is known as ‘botulism’. C. botulinum is an anaerobic, gram-positive, spore-forming rod-shaped
bacteria. The spores of C. botulinum are highly heat resistant. Seven different toxins i.e. A to
G are known to exist. Nausea, vomiting, fatigue, headache, paralysis, difficulty to talk, double
vision and sound in the ear are the usual symptoms. Symptoms develop within 18-36 h of
consuming infected food. Death occurs due to respiratory failure. Mortality rate is very high
(10 – 50%). This organism is found throughout the environment and found in the intestinal

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tract of fish, gills and viscera of crabs and shell fish. It can survive in normal cooking
temperature and grows in vaccum packed and MAP. Botulism is the problem in home canned
foods or canned foods that are improperly sterilized. Botulism is also reported from smoked,
salted and fermented fish.
C. botulinum has four groups, as well as seven antigenic variations of botulinum
neurotoxins (A–G). Botulinum toxin type A, a neurotoxin with a high fatality, is about 1,000
times more toxic than tetanus toxin. Types A, B, E, and F are mainly involved in botulism in
humans, while types C and D are mainly involved in animals. C. botulinum type E is most
common in seafoods and considered as a major concern because it can grow at very low
temperatures 3.3°C and produces little noticeable evidence of spoilage. C. botulinum-
proteolytic (mesophilic bacteria) belongs to group I, while C. botulinum-non-proteolytic
belongs to group II (psychrophilic microorganisms). Group I produces heat-resistant spores,
which are inactivated by the "Botulinum cook" (121°C/3 min) applied to canned goods with
low acid content; neurotoxins generated in this group include A, B, F, and H. Group II produces
spores that are moderately heat resistant, and the neurotoxins produced are B, E, and F. Group
II can able to grow and produce neurotoxin at refrigeration temperatures, as low as 3.0 ◦C, and
is a concern in minimally processed refrigerated foods. Foods involved in botulism are fruits
and vegetables, meats, fish, and miscellaneous combined foods (Peck, 2005).
Intoxication/Infection dose is 1 μg/kg b.w. orally, for 70 kg man 0.09 to 0.15 μg intravenously
or intramuscularly, 0.70 to 0.90 μg inhalationally. The toxin stability is 80ºC for 10 min
(function of pH and other factors); exact values are also toxin dependent. Substances in food
such as divalent cations and organic acid anions protect the toxin from heat.
Clostridium perfringens
Clostridium perfringens is an anaerobic pathogen which can able to produce several
toxins and cause enterotoxic diseases in humans and animals. Food poisoning caused by C.
perfringens may occur when foods such as meat or poultry are cooked and held without
maintaining adequate heat or refrigeration before serving. The illness is a self-limiting
gastroenteritis with an incubation period of 8-15 hours and duration of 12-24 hours. The
symptoms, which include intense abdominal cramps, gas, and diarrhea, have been attributed to
a protein enterotoxin produced during sporulation of the organism in the intestine. (Toxico-
infection)
C. perfringens are estimated to be the second most common bacterial causes of
foodborne illness in the US, causing one million illnesses each year. C.perfringens strains are
classified into seven groups A, B, C, D, E, F and G based on the different toxins it produces
(alpha, beta, epsilon, and iota). The alpha, beta, epsilon, and iota, are responsible for the tissue
lesions and the host’s death and are considered to be major toxins. Alpha toxin: The alpha
toxin, found in type A strains of C. perfringens causes gas gangrene and also hemolysis in
infected species. Beta toxin: This lethal toxin is found in C. perfringens type B and type C
strains. This toxin also results in necrosis by way of increased blood pressure, which is brought
on by the presence of catecholiamine. Epsilon toxin: This toxin is produced by type B and type
D strains of C. perfringens. It is isolated from animals, particularly sheep, goats, and cattle, but
rarely from humans. Similar to the other toxins, epsilon toxin creates pores in tissues, which
can result in leaked potassium ions and fluid leakage. Iota toxin: The iota toxin is produced
solely by type E strain of C. perfringens and is known as an AB toxin. The iota toxin can cause

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tissue death in infected individuals. Among the seven groups, C. perfringens type F is
commonly involved in foodborne toxico-infections. C. perfringens type F carries the 𝛼𝛼-toxin
gene and the cpe gene and produce CPE (C. perfringens Enterotoxin) single polypeptide of
approximately 35 kDa upon sporulation, but do not carry the structural genes for 𝛽𝛽-toxin, 𝜀𝜀-
toxin, or 𝜄𝜄-toxin (Mi, Li and McClane, 2018; Rood et al., 2018). The Infection / Intoxication
dose is 106 to 107 CFU/g of food (ingested vegetative cells produce CPE during intestinal
sporulation). The toxins produced usually in the small intestine of the host. The heat stability
of toxin is at 60 ◦C for 5 min and pH 5 to 10.
Control measures: Prevention from cross-contamination of cooked foods. Cleaning and
sanitizing food contact surfaces after being used for raw products is an effective way to control.
Staphylococcus aureus
Staphylococcus aureus is Gram positive, non-motile, facultative anaerobic, spherical
non-sporing cocci, arranged in grape-like clusters. The primary habitat of Staphylococcus
aureus is man. This organism is found in sweat, ear gum, tears, throat, ulcers, boils and nasal
cavities. Fish caught from the open sea doesn’t contain Staphylococcus aureus when the
material is taken onboard and handled by workers, contamination takes place. So, its presence
in seafood / food indicates lapse in maintaining personal hygiene
Staphylococcus aureus is considered as one of the major food borne pathogens
responsible for food poisoning outbreaks worldwide. They are enterotoxin producing
pathogenic bacterium and occurring as commensal flora of humans (Alves et al., 2014). They
have a great significance in food industry due to the ability of certain strains to produce heat
stable enterotoxin and other virulence factors which are responsible for staphylococcal food
poisoning (SFP). (Argudin et al., 2012; Tango et al., 2015). Symptoms of SFP include nausea,
violent vomiting, and abdominal cramping, with or without diarrhea within 2-4hr of
consumption (Chen et al., 2018). The minimum amount of toxins required to have symptoms
is about 1ng/g of food. SFP is widely reported on protein rich foods such as meat, dairy and
fish products which have extensive manual handling, inadequate heating and inappropriate
storage (Adam and Moss 2007). The bacteria can be killed by heat treatment, but toxin
produced is very heat resistant and remain in food even after cooking, which can cause food
poisoning.
SEs (Staphylococcus enterotoxins) belongs to a great family of staphylococcal and
streptococcal pyrogenic exotoxins, characterized by common phylogenetic relationships,
structure, function, and sequence homology. SEs function not only as potent gastrointestinal
toxins causing emesis but also as superantigens that stimulate nonspecific T-cell proliferation.
(Rajkovic et al., 2020). To date, 26 SEs and enterotoxin-like types have been described:
enterotoxins A (SEA), B (SEB), C1 (SEC1), C2 (SEC2), C3 (SEC3), D (SED), E (SEE), G
(SEG), H (SEH), I (SEI), J (SElJ), K (SElK), L (SElL), M (SElM), N (SElN), O (SElO), P
(SElP), Q (SElQ), R (SER), S (SES), T (SET), U (SElU),W(SElW)), V (SElV), X (SElX), and
Y (SElY).Enterotoxins are encoded in prophages, plasmids, or chromosomal pathogenicity
islands.
The location of the SE genes on mobile genetic elements presents an additional risk factor in
S. aureus food intoxication, due to possible horizontal gene transfer (Cafini et al., 2017;
Lindsay, 2014). The transfer of genetic elements in S. aureus has contributed to strain
variability and enhanced virulence. It is well known that S. aureus strains usually carry more

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than one SE encoding gene. The stability of toxin is SEA: 3 min at 80 ◦C, 1 min at 100 ◦C;
SEB 87 min at 99 ◦C. Stable at wide range of pH and resistant to gastric pH.
Control measures: Adequate control over the health and hygiene of fish handlers. The
fish has to be maintained at low temperature (below 5°C) during handling and processing.
Minimize time/temperature abuse of seafood, especially after cooking
Pathogenic Escherichia coli
E. coli is Gram-negative, rod-shaped, non-spore forming facultatively anaerobic
bacteria. It is commonly found in the gut of humans and warm-blooded animals. Pathogenic
strains of E. coli are transferred to seafood through sewage pollution of the coastal environment
or by contamination after harvest. Similar concerns occur if contaminated ice used for
preservation or the utensils contaminated with E. coli. Improperly cleaned boat deck, and
containers used in onboard trawlers can also act be source of contamination. There are six
categories of pathogenic E. coli, which include Enterotoxigenic E. coli (ETEC),
Enteropathogenic E. coli (EPEC), Enteroinvasive E. coli (EIEC), Enterohemorrhagic E. coli
(EHEC, Shiga toxin-producing E. coli or STEC), Enteroaggregative E. coli (EAEC or EAggEc)
and Diffusely adherent E. coli (DAEC). Among these Shiga toxin-producing E. coli (STEC)
has been associated with severe foodborne outbreaks of major public health importance in the
last years. STEC produces toxins, known as Shiga-toxins because of their similarity to the
toxins produced by Shigella dysenteriae. Shiga toxins (Stx) can be divided into two categories:
Stx1, which is identical to the toxins produced by Shigella dysenteriae 1, and Stx2, which is
around 60 % similar to Stx1. Production of one or more Shiga toxins is essential to cause
disease, but the production of Stx2 is more closely linked to the severity of the disease such as
hemolytic uremic syndrome (HUS) and HC (Farrokh, et al., 2013). STEC strains can be
classified as O157 and non-O157. Serotype O157:H7 is the most common serotype involved
in severe infections resulting to HUS and HC, and it has been linked to the majority of large-
scale outbreaks of STEC infections. Symptoms of STEC are severe diarrhea, stomach cramps,
and vomiting. Diarrhea is often bloody without fever. Symptoms typically appear 3-4 days
after eating contaminated product, but can range from 1-10 days. STEC can grow in
temperatures ranging from 7 °C to 50 °C. A recent study found that E. coli O157 strains possess
inherent genetic mechanisms which enable growth at low temperatures (< 15 °C), compared to
non-pathogenic E. coli (Vidovic et al., 2011). Some STEC can grow in acidic foods, down to
a pH of 4.4, and in foods with a minimum water activity (aW) of 0.95.
Control measures: The only effective method of eliminating STEC from foods is to
introduce a bactericidal treatment, such as heating (for example, cooking or pasteurization) or
irradiation. Basic good food hygiene practices have to be followed during handling and
processing of foods.
Vibrio cholerae
V. cholerae are Gram-negative, coma shaped, aerobic, motile rods, non-spore forming
bacteria. V. cholerae can be divided into two major groups: the cholera-causing strains of
serogroups O1 and O139, and non-O1/non-O139 V. cholerae. The non-O1 strains do not cause
diarrhoea as severe as cholera but they frequently cause extraintestinal infections. The main
virulence factor of V. cholerae O1 (Ogawa, Inaba, and Hikojima serotypes, Classical and El
Tor biotypes) and O139 is CTX toxin (Cholera toxin). It is a potent enterotoxin and causes
toxico-infections in humans. It activates the adenylyl cyclase; increases the levels of

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intracellular cAMP promoting fluid and electrolytes secretion in the intestinal epithelium,
causing diarrhea. This toxin can be identified by the presence of the ctxAB gene. Symptoms
includes profuse diarrhea, after an incubation period from 2 h to 5 days; stools have the
appearance of rice water, there is dehydration and electrolyte imbalance, which can lead to
death. The pathogen is shed in their feces for 7–14 days, which is a very serious source of
contamination since it is possible to infect others. The disease is occasionally spread through
eating raw or undercooked shellfish that are naturally contaminated.
Control measures: Proper disinfection of contact surfaces. Avoid cross contamination
of cooked products and strictly maintain the personal hygiene of seafood/food handlers
Shigella spp.
Shigella belongs to the family Enterobacteriaceae. They are gram-negative, non-motile,
and facultative anaerobic bacteria and classified in four serogroups, A (Shigella dysenteriae),
B (Shigella flexneri), C (Shigella boydii) and D (Shigella sonnei). The disease caused by
shigella is known as ‘shigellosis’, and S. dysenteriae is responsible for the more severe forms
of shigellosis. Shigella can be transmitted through direct contact (person-to-person) or
indirectly through contaminated food and water, ice, contact surface, files or food handlers who
are carriers of this organism. Shigella is naturally found in the intestinal tract of humans. The
virulence factor found in Shigella spp., is shiga toxin (Stx), which is commonly found in S.
dysenteriae serotype 1 and closely resembles Stx in Shiga toxin-producing Escherichia coli
(STEC). It is a heat labile exotoxin. It acts by inhibition of protein synthesis causing the death
of susceptable cells.
Control measures: Shigella contamination can be controlled by strictly maintaining the
personal hygiene of workers. Good sanitary and handling practice has to follow during food
processing or storage. Avoid time/temperature abuse and cold chain should be maintained.
Identify and avoid carriers from food operation and monitor for exclusion of pest.
Yersinia enterocolitica
Yersinia enterocolitica is naturally found in a wide range of foods, water, animals, and
soil. They are a biochemically diverse group capable of surviving and developing in
refrigerated temperatures. In terms of food safety, the ability to multiply at refrigeration
temperatures is quite important. It is a gastrointestinal pathogen and cause illness in humans
particularly in in young children, are fever, abdominal pain, and diarrhea, which is often
bloody. In adults, in addition to symptoms resembling appendicitis, severe parenteral forms
may appear, such as erythema nodosum, or micro abscesses in internal organs. It is transmitted
via the feco-oral route by the consumption of contaminated food or water. Y. enterocolitica can
able to produce heat-stable enterotoxins and play a key role in the pathogenesis of yersiniosis
(Samoraj, 2022). The invitro conditions required to produce enterotoxin in Y. enterocolitica
strains are 26 ºC and 37 ºC, pH7-7.5. Y. enterocolitica produce enterotoxins after reaching the
final part of the small intestine. The Yersinia stable toxins (enterotoxins) produced by Y.
enterocolitica are biologically and antigenically similar to STX1 (Shiga Toxin I) enterotoxins
produced by E. coli. Enterotoxins provoke diarrhea, which is the main cause of mortality in
yersiniosis
Detection Methods
The toxins produced by the bacteria are the most important virulence factor of
foodborne pathogens and a major contributor of foodborne related diseases. They are proteins

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or peptides that vary from one another in terms of their size, structure, toxicity, toxicological
end points, solubility, and stability, primarily in relation to the types of food matrix. These
differences influence the characteristics of required detection methods. The commonly used
methods used for detection and quantification methods for toxins in foods are bioassay method
(whole animal assay and cell culture assay), immunological method (Enzyme-linked
immunosorbent assays and reversed passive latex agglutination assay), mass spectrometry, and
molecular assays.
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