Food Bioscience 39 (2021) 100807

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Food Bioscience
journal homepage: www.elsevier.com/locate/fbio

Control of biogenic amine production and bacterial growth in fish and

seafood products using phytochemicals as biopreservatives: A review
Abderrahmane Houicher a, *, Abdelkader Bensid b, Joe M. Regenstein c, Fatih Özogul d
a
Department of Agricultural Sciences, Faculty of Science, Amar Telidji University, Laghouat, 03000, Algeria
b
Faculty of Natural Sciences and Life, Department of Agronomy, Ziane Achour University, Djelfa, 17000, Algeria
c
Department of Food Science, Cornell University, Ithaca, NY, 14853-7201, USA
d
Department of Fishing and Fish Processing Technology, Faculty of Fisheries, Cukurova University, 01330, Balcali, Adana, Turkey

A R T I C L E I N F O A B S T R A C T

Keywords: During fish spoilage, microbial growth and metabolism generate different toxic metabolites among them
Plant extract biogenic amines. Biogenic amine formation has been prevented by optimizing handling and processing condi­
Seafood tions, or by the addition of food additives up to their legal limits. However, the increased consumer demand to
Fish
reduce synthetic additives in foods because of their potential toxicity and at the same time the increased interest
Bacterial growth
Biogenic amine
for natural antimicrobials have led to increased effort to find such compounds. Several bioactive phytochemicals
are used as food ingredients to improve the shelf life and sensory properties of food products. Thus, the appli­
cation of plant extracts alone or in combination with food preservation technologies could be a good alternative
approach to improve fish and seafood quality and safety without adverse effects on human health. The present
review will summarize the information on natural antimicrobials from plant sources and discuss their different
applications in fish and seafood products with an emphasis on their mechanisms of action to prevent bacterial
growth and biogenic amines formation.

1. Introduction
Fish and seafood products are highly perishable food and usually
spoil faster than other muscle foods. The principal cause of seafood
spoilage is microbial growth and metabolism resulting in the formation
of toxic metabolites among them biogenic amines (Gram & Dalgaard,
2002). Their formation is influenced by many factors, mainly the raw
material, processing technologies, handling and storage conditions,
microorganisms, and the types of enzymes of the seafood or of the mi­
croorganisms. The control of these toxic metabolites in fish and seafood
products has frequently been undertaken because of their implication in
food poisoning outbreaks (Ruiz-Capillas and Jiménez-Colmenero,
2009). The biogenic amines are mainly produced by decarboxylation of
specific free amino acids by microbial enzymes. Many chemical food
additives are added to seafood products to prevent biogenic amines
formation by inhibiting bacterial growth or decarboxylase enzyme ac­
tivity and hence delaying amine formation. The effectiveness of food
additives depends on many processing and environmental factors, such
as concentration, other ingredients, pH, aw, temperature, atmospheric
composition, and initial microflora of the seafood (Gould, 1989; Sofos,
1989, p. 248). Although these common chemical additives are approved
in many countries, the potential health problems associated with these
synthetic compounds in foods has driven the need to replace them with
natural products. But these alternatives must continue to ensure food
safety and satisfy consumer demands. Biopreservatives including plant
extracts, bacteriocins, chitosan, and enzymes have also been used alone
or in combination with other preservation technologies to control
biogenic amine formation in fish and seafood products (Naila et al.,
2010; Prester, 2011; Viji et al., 2017; Visciano et al., 2012).
Natural plant products have been explored as potential antimicrobial
additives. Plants are rich sources of innumerable bioactive phytochem­
icals that are used not only to fortify foods, but also as food ingredients
to improve shelf life and sensory properties (Alvarez-Jubete & Tiwari,
2013). The antimicrobial compounds in plants have been grouped in
several categories including phenolic/polyphenols, terpenoids and al­
kaloids (Cowan, 1999; Tajkarimi et al., 2010; Tiwari et al., 2009; Van
Vuuren et al., 2009). This review will summarize information on the
natural antimicrobials from plant sources and discuss their different
applications in fish and seafood products and the mechanisms of their
action to prevent bacterial growth and biogenic amines formation.

* Corresponding author. Department of Agricultural Sciences, Faculty of Science, Amar Telidji University, BP 37 G, Laghouat, 03000, Algeria.
E-mail address: a.houicher@yahoo.fr (A. Houicher).

https://doi.org/10.1016/j.fbio.2020.100807
Received 7 May 2020; Received in revised form 7 September 2020; Accepted 15 November 2020
Available online 18 November 2020
2212-4292/© 2020 Elsevier Ltd. All rights reserved.
A. Houicher et al.
Fig. 1. Biogenic amines production from their amino acids precursors in fish.
2. Biogenic amines formation in seafood
Biogenic amines are formed mainly by decarboxylation of specific
free amino acids or by amination and transamination of ketones and
aldehydes. The biogenic amines of foods are histamine, putrescine,
cadaverine, tyramine, tryptamine, 2-phenylethylamine, spermine,
spermidine, and agmatine (Maijala et al., 1993; Onal, 2007; Ozogul,
2009) (Fig. 1).
Such formation involved several prerequisites: mainly the avail­
ability of free amino acids, the presence of microorganisms as producers
of decarboxylase enzymes, and the existence of conditions for bacterial
development (Marklinder & Lönner, 1992; ten Brink et al., 1990). In
general, certain concentrations of spermidine and spermine (<1
mg/100 g flesh) were initially formed in freshly caught fish depending
mainly on fish species, level of free amino acids and the conditions of
exposure to spoilage bacteria (Mackie et al., 1997; Ruiz-Capillas &
Moral, 2001). The decrease in free amino acids levels is associated with
muscle proteolysis during the spoilage of fish. Their consumption by
microorganisms as a growth substrate, gives rise to a variety of toxic
metabolites among them biogenic amines (Ochiai et al., 1990; Ruiz-­
Capillas & Moral, 2004).
Several toxic effects with potential health hazards are associated
with the consumption of foods containing high concentrations of
biogenic amines (Ruiz-Capillas and Jiménez-Colmenero, 2009), and
most of them are caused by the action of histamine (Mendes, 2009). The
implicated fish products most often belong to the Scombridae and
Scomberesocidae families (“scombroid”), but non-scombroid species
can also be involved in this food-borne intoxication. Histamine does not
appear to be the only causative agent of this intoxication; other amines
such as tyramine, putrescine and cadaverine are also implicated as po­
tentiators of histamine toxicity, i.e., although not intoxicating on their
own, they will make the effect of histamine worse (Halász et al., 1994;
Rice et al., 1976). The most common symptoms of histamine fish
poisoning result from their action on the cardiovascular system
involving manifestations such as a vasodilating effect, producing low
blood pressure and headaches, reddening of the skin, edemas and rashes,
and a burning or peppery taste in the mouth. These are seen along with
typical allergic reactions, diarrhea, and abdominal cramps (Bardocz,
1995; Lehane & Olley, 2000; Taylor, 1986). Tyramine has been shown to
2
Food Bioscience 39 (2021) 100807
be a biologically vasoactive amine that is considered as the initiator of a
hypertensive crisis, while putrescine and cadaverine can react with ni­
trite to form potentially carcinogenic nitrosamines (Shalaby, 1996; Huis
in’t Veld et al., 1990).
The US Food and Drug Administration (FDA) recommended not only
using histamine as a quality control index to detect fish spoilage but to
develop defect action levels. However, other biogenic amines associated
with fish decomposition among them agmatine and cadaverine may be
used for these purposes (e.g., by the European Union) (Commission
Regulation (EC), 2005) All three of these amines have been used as in­
dicators of autolytic changes responsible for the loss of fish freshness and
proposed as control indices in fish and seafood products treated with
vacuum or modified atmospheres (Paarup et al., 2002; Ruiz-Capillas &
Moral, 2001; Yamanaka et al., 1987). Unfortunately biogenic amines are
thermally stable compounds, although they therefore can be useful in­
dicators of poor-quality raw material in preserved fish products such as
canned fish (Huss, 1995). In the European Union, the average histamine
(m) of nine samples should be below 100 mg/kg for fishery products
from fish species associated with a high amount of histidine. Two of the
nine samples are allowed to have a histamine concentration between
100 and 200 mg/kg but no fish samples may exceed the limit (M) of 200
mg/kg. For fishery products which have undergone enzyme maturation
treatment in brine, manufactured from fish species associated with a
high amount of histidine, the same regulation stipulated the level of 200
mg/kg as legal limit of histamine in nine fish samples, but no samples are
allowed to have the maximum concentration of 400 mg/kg (Commission
Regulation (EC), 2005). For the US, the FDA (Food and Drug Adminis­
tration (FDA), 2001) has set a legal limit of 50 mg of histamine/kg of
flesh, while 500 mg of histamine/kg is considered a potential health
hazard. In other countries such as Australia and New Zealand, 200
mg/kg are regarded as a safe legal limit of histamine concentration for
health, whereas 100 mg of histamine/kg are considered as the limit in
South Africa (Auerswald et al., 2006). It would be beneficial for fish and
seafood trade if the various governments could agree to a single stan­
dard, possibly through the mechanism of Codex Alimentarius, the World
Health Organization and the Food and Agricultural Organization of the
United Nations’ effort to establish global standards.
A. Houicher et al. Food Bioscience 39 (2021) 100807

Table 1 Table 1 (continued )

The major amine forming bacteria in fish and fish products. Amine forming Implicated Main amines References
Amine forming Implicated Main amines References bacteria sefood formed
bacteria sefood formed
Gram negative
Gram negative
smoked tuna,
Morganella Fish stored Histamine, Kim et al. (2003); fresh tuna
morganii under aerobic putrescine, Middlebrooks et al. Photobacterium Raw fish and Histamine Kanki et al. (2007)
conditions cadaverine (1988); Frank et al. damselae dried fish
(1985); Lopez-Sabater products
et al. (1996) Vibrio Fish stored Histamine Middlebrooks et al.
Klebsiella Fish stored Histamine, Kim et al. (2003); Frank alginolyticus under aerobic (1988); Frank et al.
pneumoniae under aerobic putrescine, et al. (1985) conditions (1985)
conditions cadaverine,
Gram positive
tyramine
Hafnia alvei Fish stored Histamine, Kim et al. (2003); Staphylococcus Salted fish Histamine Hernández-Herrero et al.
under aerobic putrescine, Lopez-Sabater et al. epidermidis products (1999)
conditions cadaverine, (1996); Lehane and Olley Staphylococcus Salted fish Histamine Hernández-Herrero et al.
(2000) capitis products (1999)
Citrobacter Raw fish and Histamine Kim et al. (2003); Staphylococcus Cooked fish Histamine Naila et al. (2011)
freundii fish products Lopez-Sabater et al. hominis paste
(1996) Clostridium Fermented fish Histamine, Middlebrooks et al.
Raoultella Raw fish and Histamine Kim et al. (2003) perfringens products putrescine, (1988)
planticola fish products cadaverine
Raoultella Raw fish and Histamine Kim et al. (2003) Bacillus Cooked fish Histamine Naila et al. (2011)
ornithinolytica fish products polyfermenticus paste
Serratia fonticola Fish stored Histamine, Kim et al. (2003); Bacillus Cooked fish Histamine Naila et al. (2011)
under aerobic putrescine, Lopez-Sabater et al. massiliensis paste
conditions cadaverine (1996) Bacillus Fermented fish Histamine Tsai et al. (2006)
Serratia Fish stored Histamine, Kim et al. (2003); coagulans products
liquefaciens under aerobic putrescine, Lopez-Sabater et al. Bacillus Fermented fish Histamine Tsai et al. (2006)
conditions cadaverine (1996) megaterium products
Kluyvera Iced-preserved Histamine, Fadhlaoui-Zid et al. Enterococcus Iced-preserved Tyramine Fadhlaoui-Zid et al.
intermedia sardine and putrescine, (2012) durans sardine and (2012)
mackerel cadaverine mackerel
Enterobacter Iced-preserved Putrescine, Fadhlaoui-Zid et al. Tetragenococcus Salted fish Histamine Kimura et al. (2001)
asburiae sardine and cadaverine (2012) muriaticus products
mackerel
Escherichia coli Raw fish and Histamine Lopez-Sabater et al.
fish products (1996) 3. Bacterial growth and amine forming bacteria
Enterobacter Fish stored Histamine, Kim et al. (2003)
aerogenes under aerobic putrescine,
conditions cadaverine
The microflora of fish and seafood products are a reflection of the
Enterobacter Fish stored Histamine, Houicher et al. (2013); microorganisms present in newly caught fish and the microbial
cloacae under aerobic putrescine, Kim et al. (2003); contamination during handling, processing, and storage. Normally, the
conditions cadaverine Lopez-Sabater et al. muscles of healthy fish are considered to be sterile, but the surfaces such
(1996)
as skin, gills, and gastrointestinal tract contain varying numbers of mi­
Proteus vulgaris Fish stored Histamine, Kim et al. (2003);
under aerobic putrescine, Ababouch et al. (1991) croorganisms (104 CFU/cm2 in the skin, 106 CFU/g in the gills, and up to
conditions cadaverine 108 CFU/g in the digestive tract) (Austin, 2002). The microflora of fish is
Proteus mirabilis Fish stored Histamine, Houicher et al. (2013); dominated by Gram negative species belonging to the genera Pseudo­
under aerobic putrescine, Kim et al. (2003); monas, Acinetobacter, Moraxella, Flavobacterium and Shewanella. Mem­
conditions cadaverine Ababouch et al. (1991)
bers of the Aeromonadaceae (Aeromonas spp.) and the Vibrionaceae
Providencia Raw fish and Histamine Houicher et al. (2013);
stuartii fish products Ababouch et al. (1991) (Vibrio and Photobacterium) are also common in the aquatic environment
Acinetobacter Raw fish and Histamine Middlebrooks et al. and typical of the fish flora. Gram positive organisms can also be
lowffi fish products (1988) observed in varying proportions, including Micrococcus, Bacillus, Lacto­
Pseudomonas Fish stored Putrescine, Lopez-Sabater et al.
bacillus, Clostridium, and coryneforms (Huss, 1995). Pathogenic bacteria
putrefaciens under aerobic cadaverine (1996)
and vacuum such as Clostridium botulinum, Plesiomonas shigelloides, pathogenic Vibrio
conditions spp., and Aeromonas spp. Can be part of the natural microflora of fish or
Pseudomonas Fish stored Putrescine, Lopez-Sabater et al. introduced onto fish during handling, processing and storage such as
putida under aerobic cadaverine (1996) Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, Yersinia
and vacuum
enterocolitica, Salmonella spp., Bacillus spp., and Shigella spp. (Davies
conditions
Aeromonas Raw fish and Histamine, Middlebrooks et al. et al., 2001; Huss, 1997).
hydrophila fish products putrescine, (1988) The major cause of spoilage of fresh fish and fish products is either
cadaverine the microbial growth directly or the bacterial enzymes and their meta­
Plesiomonas Fish stored Histamine Lopez-Sabater et al.
bolism of the fish nutrients (Huss, 1995). The important factors affecting
shigelloides under aerobic (1996)
conditions
microorganism growth are storage time and temperature, which in­
Morganella Tuna in chilli- Histamine Emborg et al. (2005) cludes the production of amino acid decarboxylase enzyme necessary for
psychrotolerans sauce, cold- the formation of biogenic amines. Prolonging the time and/or increasing
smoked tuna the temperature during storage increases the biogenic amines concen­
Photobacterium Dried sardines, Histamine Kanki et al. (2007);
trations. Except for spermidine and spermine, the levels of biogenic
phosphoreum tuna in chilli- Emborg et al. (2005)
sauce, cold- amines increase progressively throughout fish storage in ice (Ruiz-Ca­
pillas and Jiménez-Colmenero, 2009), and this production is related to
the activity of both mesophilic and psychrotrophic bacteria. Thus,

3
A. Houicher et al.
starting with clean raw materials and then keeping fish at a low tem­
perature throughout the storage and processing is the most effective way
to prevent biogenic amines formation (Huss, 1995).
Several Gram negative and Gram positive bacteria are implicated in
the formation of biogenic amines. The strongest histidine decarboxylase
activity is observed with Morganella morganii followed by Klebsiella
pneumoniae, Hafnia alvei, and some strains of Enterobacter aerogenes and
E. cloacae (Kim et al., 2003). Morganella psychrotolerans and Photo­
bacterium phosphoreum, are strong histamine-producing psychrotolerant
bacteria. They can also produce toxic concentrations of biogenic amines
in seafood (Dalgaard et al., 2008; Emborg et al., 2005). Vibrio spp.,
Staphylococcus spp., and Pseudomonas spp. have also been identified as
histamine-producing bacteria in fermented fish (Yankah et al., 1993;
Yatsunami & Echigo, 1993). Gram positive bacteria, however, are
frequently implicated in tyrosine decarboxylase activity (Bover-Cid &
Holzapfel, 1999). Table 1 is a list of amine forming bacteria associated
with fish.
In general, biogenic amines are thermostable and hence the presence
of biogenic amines in canned fish indicates that the raw material has
been spoiled before thermal processing (Huss, 1995; Shalaby, 1996). In
fermented fish products, stages in fermentation may have long pro­
cessing time without adequate temperature control, and consequently
the increase of biogenic amine concentrations at higher fermentation
temperatures, especially histamine followed by phenylethylamine
(Ruiz-Capillas and Jiménez-Colmenero, 2009). In addition, the control
of biogenic amine formation in fish using NaCl requires that initially
these compounds had not been formed in the raw material prior to the
addition of salt and the added amount of NaCl must be also sufficient to
reduce amine forming bacteria growth (Dalgaard et al., 2008). The
application of protective atmospheres, in general, reduces biogenic
amines formation (except spermidine and spermine). This is mainly due
to the effect of the gas mixtures on microbial growth and therefore on
the amino acid decarboxylase enzyme (Ruiz-Capillas and
Jiménez-Colmenero, 2009). However, Photobacterium phosphoreum and
the CO2-resistant strains of P. phosphoreum have been identified as
responsible for the production of biogenic amines in vacuum-packed
cold-smoked salmon (Jorgensen et al., 2000) and the spoilage of
modified atmosphere packaged (MAP) cod (Emborg, Laursen, Rathjen,
& Dalgaard, 2002), respectively. High pressure processing technology
also allows microbial inactivation and ensures product safety. Paarup,
Sanchez, Pelaez, and Moral (2002) reported that the application of
moderate pressures (150–200 MPa) reduces the rate of agmatine for­
mation, whereas pressurization at 400 MPa inhibits histamine formation
and keeps putrescine formation low, but does not stop tyramine for­
mation. Moreover, fish irradiation is a physical method that exposes fish
to high ionization energy gamma-rays to extend shelf life and improve
their safety and quality. A combination of vacuum packaging and a low
dose of γ-irradiation (1.5 kGy) was more efficient in reducing histamine,
putrescine and cadaverine in chub mackerel than vacuum packaging
alone (Mbarki et al., 2009). The prevention of bacterial growth and
control or inhibition of enzymatic activity of amine decarboxylase
bacteria necessitates suitable raw material, together with the optimi­
zation of process and storage conditions.
4. Phytochemicals and their antimicrobial effects
The essential oils and extracts from leaves, flowers and flower buds
or other parts of the plant are the major sources of antimicrobial com­
pounds (Nychas, 1995; Shelef, 1984). These active compounds are
phenolics, terpenes, aliphatic alcohols, aldehydes, ketones, acids, and
isoflavonoids (López-Malo Vigil et al., 2005), which have long been
classified as Generally Recognized as Safe (GRAS) by the US FDA
(Kabara, 1991), and their use as antimicrobial agents would provide
beneficial effects for health and food preservation.
Phenolic compounds can be divided into two major categories:
phenolic acids and flavonoids. The phenolic acids are benzoic or
4
Food Bioscience 39 (2021) 100807
cinnamic acid derivatives, while the flavonoids are largely anthocyanins
and tannins (Dykes & Rooney, 2006). Several studies have shown the
effectiveness of phenolic compounds in controlling and/or inhibiting the
growth of microorganisms with a wide antimicrobial spectrum, among
them thymol, cinnamic aldehyde, and eugenol (Beuchat, 2001; Lucera
et al., 2012; Takó et al., 2020). In addition, the inhibitory effect of
phenolic compounds included p-hydroxy benzoic, p-coumaric acids,
caffeic, vanillic, syringic, protocatechuic, quercetin and oleuropein
against the growth of Klebsiella pneumoniae, E. coli, Bacillus cereus,
Aspergillus parasiticus, and Aspergillus flavus was reported (Aziz et al.,
1998). The efficacy of natural phenolic compounds to inhibit the growth
of Gram negative and Gram positive foodborne bacteria was also
measured by Cetin-Karaca and Newman, (2015a; 2015b). These com­
pounds have varying antimicrobial activities against foodborne patho­
gens, indicating their great potential to be used as natural preservatives
during long term storage.
Terpenes are the second group of antimicrobial compounds and the
largest group of natural products occurring as a constituent of many
essential oils (Burt, 2004; Graβman, 2005). Their classification is based
on the number of isoprenoid units present in their structure, which
consist of monoterpenes (two units), sesquiterpenes (three units),
diterpenes (4 units), sesterterpenes (5 units), triterpenes (6 units), and
tetraterpenes (8 units) (Ashour et al., 2010). Many terpenes are known
to be active against a variety of microorganisms, including Gram
negative and Gram positive bacteria and fungi (Cowan, 1999; Nakatani,
1994). Trombetta et al. (2005) reported the efficacy of three mono­
terpenes (linalyl acetate, (+)-menthol, and thymol) against E. coli and
S. aureus. Various diterpenes extracted from Salvia species showed
antibacterial activities against a variety of organisms such as E. faecalis,
B. subtilis, S. aureus, S. epidermis, E. coli, and P. mirabilis (Ulubelen, 2003).
Sesquiterpene drimanes have also shown strong antibacterial and anti­
fungal activity (Lunde & Kubo, 2000; Rastogi et al., 1998). In addition,
different terpenes such as carvone, linalool, 1,8-cineol, δ-3-carene,
spathulenol, α-pinene, β-pinene, β-myrcene, and germacrene showed
antifungal activity toward many pathogenic fungi species (Houicher et
al, 2016a, 2016b, 2018). However, the use of essential oils in food as
preservatives is often limited due to flavour considerations (Lambert
et al., 2001).
Among the antimicrobial compounds that are produced by plants,
alkaloids figure as a prominent class among the nitrogen-containing
secondary metabolites (Campos-Vega & Oomah, 2013). The isoquino­
line and indole alkaloids are the two major classes of alkaloids, syn­
thesised principally from the aromatic amino acids such as tryptophan,
tyrosine and arginine and also aspartic acid (Campos-Vega & Oomah,
2013). Many alkaloids are known to have antimicrobial activity, which
has been investigated (Verpoorte, 1998). For example, caffeine at a
concentration of 0.5% has shown significant growth inhibition against
E. coli O157:H7 (Ibrahim et al., 2006). Berberine, a traditional plant
alkaloid, is more active against Gram positive bacteria including
S. aureus and S. epidermidis than against Gram negative bacteria (Vud­
danda et al., 2010). Erdemoglu et al. (2007) reported that Lupinus
angustifolius alkaloid extract showed significant activity toward
P. aeruginosa, S. aureus, and B. subtilis while it had moderate activity
against Candida krusei and C. albicans. Although numerous alkaloids
from plants are characterized pharmacologically and are used as clinical
drugs, some of them have also been used as antimicrobials in food (Hintz
et al., 2015).
Other antimicrobial compounds such as allicin, methyl methane
thiosulfonate, and glucosinolates have long been recognized for their
antimicrobial activity against Gram positive and Gram negative bacteria
as well as fungi (Shao et al., 2011). Some minor classes of natural
products including decarboxymethyl elenolic acid (EDA), hexanal,
benzyl acetate, and estragole have also been shown to have antimicro­
bial activity that may be used in food preservation (Shao et al., 2011).
A. Houicher et al. Food Bioscience 39 (2021) 100807

Table 2
Examples of application of essential oils and crude extracts in seafood to control biogenic amines formation.
Plant name Extract Seafood matrix Storage conditions Decreased amines References

Mentha spicata Essential oil Sciaenops ocellatus Under aerobic conditions/4 ± 1 C ◦

Histamine, putrescine, cadaverine Cai, Cao, et al.
(2015)
Rosmarinus Essential oil Oncorhynchus mykiss Under aerobic conditions/4 ± 1 C ◦
Histamine, tyramine, cadaverine, Peiretti et al.
officinalis putrescine (2012)
Origanum vulgare Essential oil Cyprinus carpio Under vacuum packaging/3.5 ◦ C Tyramine, cadaverine, putrescine, Křížek et al. (2018)
phenylethylamine
Thymus vulgaris Essential oil Cyprinus carpio Under vacuum packaging/3.5 ◦ C Tyramine, cadaverine, putrescine, Křížek et al. (2018)
phenylethylamine
Cinnamomum Essential oil Ctenopharyngodon Under aerobic conditions/4 ± 1 C ◦
Putrescine, cadaverine Huang et al. (2017)
tamala idellus
Peels of lemon Essential oil Sardina pilchardus Salting and ripening conditions Histamine Alfonzo et al.
(2017)
Mentha spicata Ethanolic extract Sardina pilchardus Under vacuum packaging/3 ± 1 ◦ C Histamine, tyramine, cadaverine Houicher et al.
(2015)
Artemisia Ethanolic extract Sardina pilchardus Under vacuum packaging/3 ± 1 ◦ C Histamine, tyramine, cadaverine Houicher et al.
campestris (2015)
Rosmarinus Ethanolic extract Sardina pilchardus Under vacuum packaging/3 ± 1 C ◦
Histamine, cadaverine, putrescine Özogul et al. (2011)
officinalis
Salvia officinalis Ethanolic extract Sardina pilchardus Under vacuum packaging/3 ± 1 ◦ C Histamine, cadaverine, putrescine Özogul et al. (2011)
Rosmarinus Water-soluble extract Sardinella aurita Under ice/4 ◦ C Histamine, putrescine Özyurt et al. (2012)
officinalis
Rosmarinus Crude extract Haliotis discus hannai Sodium alginate coating/under Putrescine, cadaverine and tyramine Hao et al. (2017)
officinalis Ino chill conditions
Punica granatum Aqueous extract/ Aristichthys nobilis Under aerobic conditions/4 ◦ C Putrescine, cadaverine Zhuang et al.
ethanolic extract (2019)
Camellia sinensis Aqueous extract Engraulis encrasicolus Under marination and vacuum Histamine, tyramine, cadaverine Bilgin Fıçıcılar
packaging/4 ◦ C et al. (2018)
Laurus nobilis Aqueous extract Engraulis encrasicolus Under marination and vacuum Histamine, tyramine, cadaverine, Bilgin Fıçıcılar
packaging/4 ◦ C phenylethylamine, tryptamine et al. (2018)
Melissa officinalis Ethanolic extract Engraulis encrasicolus Under vacuum packaging/2 ± 1 ◦ C Histamine, tyramine Özogul et al. (2017)
Lavandula Ethanolic extract Engraulis encrasicolus Under vacuum packaging/2 ± 1 ◦ C Histamine, tyramine Özogul et al. (2017)
stoechas
Thymus vulgaris Supercritical fluid Sardinella aurita Fermentation and under vacuum Histamine, cadaverine, putrescine Kuley et al. (2018)
extract packaging/3 ± 1 ◦ C
Laurus nobilis Supercritical fluid Sardinella aurita Fermentation and under vacuum Histamine, cadaverine, putrescine Kuley et al. (2018)
extract packaging/3 ± 1 ◦ C
Helichrysum Ethanolic extract Oncorhynchus mykiss Under vacuum packaging/2 ± 1 ◦ C Histamine, cadaverine, putrescine Özogul et al. (2013)
Viscum album Ethanolic extract Oncorhynchus mykiss Under vacuum packaging/2 ± 1 ◦ C Histamine Özogul et al. (2013)

5. Effect of phytochemicals on biogenic amines formation
Several studies have shown the efficiency of natural plant extracts
and their active compounds to improve the overall quality and extend
the shelf life of various food model systems, especially seafood. Essential
oils and crude extracts or some of their active compounds are added
alone or in combination with different preservation methods to prevent
bacterial growth and to control biogenic amines formation in seafood
(Table 2).
Treatment of red drum (Sciaenops ocellatus) fillets with spearmint,
clove, and cumin essential oils not only maintained the sensory quality
of fish during storage, but was also able to lower microbial counts and
biogenic amines content, especially histamine, putrescine, and cadav­
erine (Cai, Cao, et al., 2015). Cinnamon bark oil treatment was effective
in extending the sensory shelf life of grass carp fillets stored at 4 ± 1 ◦ C
(Huang et al., 2017). This treatment also inhibited microbial growth and
delayed the increase of cadaverine and putrescine during chilled stor­
age. Treatment of minced rainbow trout (Oncorhynchus mykiss) muscle
with rosemary oil also led to low biogenic amine contents, especially
histamine, tyramine, cadaverine, and putrescine (Peiretti et al., 2012).
Křížek et al. (2018) studied the biogenic amines formation in vacuum
packed fillets of carp (Cyprinus carpio) treated with two essential oils
from thyme and oregano. They observed that these oils were effective in
suppressing the formation of cadaverine, tyramine, putrescine, and
phenylethylamine. However, the effects of essential oils on biogenic
amines formation and amine forming bacteria growth in fish matrix is
limited due to flavour considerations; therefore several studies have
focused on the use of different crude extracts or some of their active
compounds as biopreservatives in seafood. For example, mint (Mentha
spicata) extract treatment combined with vacuum packaging signifi­
cantly decreased the biogenic amines contents in sardine (Sardina pil­
chardus) fillets, while the addition of 1% of Artemisia (Artemisia
campestris) extract kept histamine-forming bacteria at low levels until
sensory rejection (Houicher et al., 2015). Özogul et al. (2011) reported
the positive effects of sage tea (Salvia officinalis) and rosemary (Ros­
marinus officinalis) extracts to decrease histamine, cadaverine, putres­
cine, and trimethylamine accumulation in vacuum packed sardine
fillets. Later, Özogul et al. (2013) observed that the addition of straw­
flower extract at 0.5% (w/v) extended the shelf life of fish fillets,
decreased biogenic amine accumulation, and kept lactic acid bacteria
and Enterobacteriaceae levels low. In another study, icing along with
rosemary extract was used by Özyurt et al. (2012) with sardine (Sardi­
nella aurita) to study its effect on biogenic amine formation. They
observed that this treatment not only led to a significant extension in the
shelf life of fish, but also maintained biogenic amine content at low
levels, especially histamine and putrescine. Mah et al. (2009) studied the
effects of 6 spices, garlic, ginger, green onion, cinnamon, clove, and red
pepper, on biogenic amine production in Korean salted and fermented
anchovy. The garlic extract treatment showed the highest antimicrobial
activity against Bacillus licheniformis strains, a strong amines former, and
the greatest inhibitory effect on biogenic amine contents. However, less
or no effect in decreasing biogenic amine production was observed for
the other spice extracts tested. Recently, Zhuang et al. (2019) showed
that both aqueous and ethanolic pomegranate peel extracts treatments
inhibited the growth of spoilage bacteria, especially Aeromonas and
Pseudomonas, and suppressed the production of biogenic amines in
bighead carp (Aristichthys nobilis) fillets stored at 4 ◦ C. Moreover, the
addition of green tea (Camellia sinensis) and bay leaf (Laurus nobilis)

5
A. Houicher et al.
Fig. 2. Mechanisms of action of natural antimicrobials form plant sources.
extracts in marinated anchovies reduced the microbial load of the
product (Bilgin Fıçıcılar et al., 2018), while the treatment of the Euro­
pean anchovy with 1% lemon balm or lavender ethanol extracts
decreased most biogenic amines, especially histamine (Özogul et al.,
2017).
Some active compounds are also added as biopreservatives to control
biogenic amines formation and to prevent bacterial growth in seafood
products. Qian et al. (2018) investigated the effect of active compounds
(0.05 g/L quercetin, 0.025 g/L cinnamic acid, and 0.025 g/L 4-hexylres­
orcinol) in combination with modified atmosphere packaging (MAP)
(80% CO2/10% N2/10% O2) on the productions of biogenic amines in
Pacific white shrimp. These authors concluded that MAP reduced psy­
chrotrophic bacterial counts and decreased most biogenic amines,
except for tyramine, whereas the combined treatment led to lower
bacterial counts and total biogenic amines, especially tyramine. In a
similar study, application of tea polyphenols in combination with 6-gin­
gerol in shrimp paste not only reduced microorganism counts, but also
inhibited biogenic amines accumulation and maintained paste appear­
ance for 160 days of storage at ambient temperature (Cai, Liu, et al.,
2015). Del Nobile et al. (2009) also observed that the combination of
thymol (110 ppm) with three different modified atmosphere packaging
improved the microbial acceptability of fresh blue fish burgers for 28
days of storage, while no biogenic amines were accumulated in the
samples during storage at 4 ◦ C.
However, phytochemical stability is affected by many variables,
including temperature, time of processing, light, water activity (aw),
enzymes, structure, atmospheric composition, and storage conditions,
suggesting that these molecules are unstable and highly susceptible to
degradation and decomposition (Yang et al., 2013). For example, the
stability of phenolic compounds is highly pH dependent and varies
depending on the structural conformation. Flavan-3-ols show high
storage stability with acidic conditions but are unstable at neutral pH
(Chen et al., 1998; Xu et al., 2003; Zhu et al., 1997) indicating that the
protective effect on polyphenolics is higher at lower pH (Gallarate et al.,
6
Food Bioscience 39 (2021) 100807
1999). Moreover, almost half of the phenolics were lost within the first
hour of storage at 65% relative humidity (Negi, 2013), while the three
most predominant phenolic compounds in tea showed higher stability at
lower temperature in the dark, indicating that both temperature and
light were significant factors influencing phenolic stability during stor­
age (Callemien & Collin, 2007). Some phenolic acids are heat-sensitive,
e.g., caffeic acid, which could be reduced during heat processes. Others
susceptible to thermal breakdown include p-coumaric and ferulic acids
(Huang & Zayas, 1991; Pisarnitskii et al., 1979). Packaging can also
affect quality of phytochemicals and phytochemical-containing foods by
influencing browning, flavour, and nutrient losses during storage.
Microencapsulation and nanoencapsulation are promising techniques
that can be potentially used to incorporate phytochemicals into edible
coatings, leading to increased stability and viability for longer durations
(Negi, 2013).
6. Mechanisms of action of natural antimicrobials from plant
sources
Biogenic amines are produced by the amino acid decarboxylase en­
zymes of bacteria naturally present in seafood products. Natural anti­
microbials may be used to control or inhibit spoilage and pathogenic
bacteria implicated in the formation of fish biogenic amines. However,
their mechanism of action is not fully elucidated, due to the variations in
the chemical composition and structure of these compounds. For
example, the lipophilic properties and mixtures of active compounds
may increase the efficiency of the essential oils. The membrane
disruption by lipophilic compounds can inhibit the different enzymatic
activities, mainly protein translocation, electron transport, and phos­
phorylation, which then destroy the cell membrane integrity and lead to
microbial death (Dorman & Deans, 2000; Gyawali & Ibrahim, 2014).
Terpenes, the main compound of essential oils, can also disrupt the lipid
structures of the bacterial membrane and damage the membrane’s
integrity and dissipate the proton motive force (Sikkema et al., 1995;
A. Houicher et al.
Kararli et al., 1995) (Fig. 2). The effectiveness of terpenes is also influ­
enced by the position of the –OH group, which acts as a proton
exchanger that can lead to cell death when it is in the right position
(Gyawali & Ibrahim, 2014). The antimicrobial activity of other phenolic
compounds also depends on their hydroxyl groups (–OH) and the
number of double bonds, and the size of added alkenyl or alkyl group,
which can interact with the bacterial membrane causing its disruption
and leakage of cellular contents which may lead to cell death (Fig. 2).
These groups can also alter the cell metabolism of microorganisms by
binding the active site of enzymes (Xue et al., 2013; Gyawali & Ibrahim,
2014; Lai & Roy, 2004). Vattem et al. (2005) explained that the possible
antimicrobial action of phenolic acids is related to the
hyper-acidification at the bacterial cytoplasmic membrane by dissocia­
tion of phenolic acids, which may alter the cell membrane function,
increase its permeability, and affect ATP synthesis. Several studies have
also shown the effectiveness of flavonoid compounds as antibacterial
agents. Inhibition of DNA and RNA synthesis, inhibition of energy
metabolism, inhibition of cytoplasmic membrane function, and alter­
ation of the membrane permeability are the main antibacterial mecha­
nisms of flavonoids (Xie et al., 2015; Tim Cushnie & Lamb, 2005)
(Fig. 2). The biological activity of tannins is related mainly to the
configuration and mass of their ortho-phenolic hydroxyl groups (Scho­
field et al., 2001). Alkaloids can also act through different mechanisms
among them inhibition of cell division, respiratory inhibition by binding
bacterial enzymes, disruption of cell membranes, and inactivation of
virulence genes (Othman, Sleiman, & Abdel-Massih, 2019).
From these observations, the active sites of cell membrane and en­
zymes are the major targets of natural antimicrobials which may
destabilize the cell membrane integrity, inhibit the different enzymatic
activities, and lead to microbial death. These mechanisms could explain
the efficiency of natural plant extracts and their active compounds to
delay bacterial growth and decrease biogenic amines formation in fish
matrix.
7. Conclusions
Biogenic amines production in seafood depends mainly on amino
acid precursors and the presence of amino acid decarboxylase enzymes
from spoilage and pathogenic bacteria. The control of these hazardous
amines necessitates the optimization of handling and processing con­
ditions, but other alternatives such as the addition of different food
additives at or below legal limits can be used and is gaining popularity.
Thus, the available data shows the efficiency of natural plant extracts
and their active compounds to delay or inhibit bacterial growth and
decrease biogenic amines production at low levels in fish and seafood
products. The use of natural antimicrobials from plants alone or in
combination with other preservation technologies could be a good
alternative approach to improve seafood quality and satisfy the con­
sumer’s demands without adverse effects on human health and even
possible beneficial effects. However, a complete evaluation of the
toxicity and safety of these natural antimicrobials is needed, together
with regulatory approval before their application in any food industry as
biopreservatives.
Declaration of competing interest
The authors declare that there are no conflicts of interest in this
review.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.fbio.2020.100807.
7
Food Bioscience 39 (2021) 100807
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