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1
HUMAN HEALTH RISKS ASSOCIATED WITH CHEMICAL AND
MYCROBIOLOGICAL CONTAMINANTS IN FISH – A Mini Review
Ana-Andreea CIOCA1*, Ioana -Raluca BALLA1, Marian MIHAIU1, Liora Mihaela
COLOBATIU2
1Department of Animal Husbandry and Food Safety, University of Agricultural Sciences and
Veterinary Medicine, 3 -5 Calea Mӑnӑṣtur Street, 400372, Cluj -Napoca, Romania
2Department of Medical Devices, Iuliu Hațieganu University of Medicine and Pharmacy, 8 Babe ș
Street, 400012, Cluj -Napoca, Romania
*Corresponding author email: [anonimizat]
Abstract
Fish meat consumption has gained a lot of popularity in Europe in the last years. It is considered to be a great alternative
for red meat because it provides large amounts of Omega -3 fatty acids and vitamin D. These components lower the risk
of cardiovascu lar disease, reduce the risk of autoimmune diseases, are essential for growth and development, can
contribute to mood elevation and can prevent cognitive decline, and eye disease. Unfortunately the benefits can sometimes
be accompanied by a risk associated with chemical and microbiological contaminants.
The aim of this paper is to review some recently published studies concerning the groups of chemical compounds and
bacteria found in fish meat, which can have negative effects on human health. In order to ra ise awareness, aspects related
to dangerous persistent organic pollutants and zoonotic bacteria are described. The frequency of encountering them is
discussed, the ways in which they can reach the human body are specified and a critical comparison of their consequences
is performed.
Keywords : chemical contaminants, fish, human health, microbiological contaminants.
2
INTRODUCTION
Worldwide, fish and fish products are
appreciated for being an important source in the
diets of human beings. This is the reason for
which the demand of fish meat has increased in
the last decades around the world, forcing us to
guarantee safe, edible fish in the international
trade market.
Fish and fish products are an important source
of ω-3-polyenic acids with five and six double
bonds (Fangkai Han, 2016) . These components
are commonly called fatty acids and represent a
valuable point of supply in nutrients, highly
recommended in our daily nutrition (Hellberg et
al., 2012; Ibrahim et al. 2011).
Despite the fact that fish meat is recommended
to prevent a serie of disorders or illnesses, or to
secure some vitamins and nutrients which are
mostly needed in certain maladies (Hellberg et
al., 2012) , this special category of white meat
carries a hard burden with it in our current time
(Lee et al. , 2010) . Dangerous chemical
contaminants and bacteria are often present in
fish muscle, adipose tissue or even organs
(Fernandes et al., 2015) . This mixed load partly
exists due to human interference in natural
ecosystems, especially when referring to
chemical compounds.
A previous estimated growth of world
population, guided humans towards a less
healthy approach of the contaminants -nature
situation on the long term (Nicolopoulou –
Stamati et al., 2016) . The massive use of
chemicals in the past, such as fertilizers and
pesticides in the expansion and protection of
crops which were thought to p rovide the
necessary food for all people, was discovered
decades ago to have negative effects on human
health (Kim et al., 2016) . Their initial beneficial
role in boosting plants used for animal and
human nourishment – to attai n more animal
products and sustain life on the planet – turned up
creating concerning issues starting from the base
of the food chain pyramid to the top (Binukumar
and Gill, 2011) (Ene et al., 2014) .
Persistent Organic Pollutants (POPs) is the name
attributed to organochlorine compounds,
polychlorinated biphenyls (PCBs) and other
chemical groups due to their persistence in the
environment and their bioaccumulation
characteristic. Studies have shown tha t POPs have the ability to cross from soil and water
(Neamtu et al., 2009) to plants and animals
(Shakeri et al., 2015) to which they clearly cause
disturbances (Berg et al., 20 16), so that they can
make their way up to superior organisms such as
humans (Fig 1 ).
Fig 1 Pyramid of food chain
The risk for humans is mainly the chronic
toxicity, following the ingestion of small
quantities of POP residues from fish, fish
products and other animal origin products
(Carpenter, 2011) . Acute toxicity can also
appear in human subjects who make direct
contact with pesticides through inaccurate
handling (Sumon et al., 2016) .
Animals tend to concentrate the POPs from
water and feed in their adipose tissue (e.g.
organochlorine compounds and PCBs) and pass
them to humans through food ingestion
(Fernandes et al., 2015) .
Once entered in the human body, the residues
start perturbing the normal function of the
organism and focus their action on enzyme
systems, on vitamins and hormones (endocrine
disruptors), as well as their carcinogenic
activity.
Additionally, humans can come in direct contact
or through the consumption of raw fish, with a
wide range of harmful bacteria. Such biological
contaminants can also be accumulated in fish
tissue or body surface and therefore to be
transmitted to humans along the food chain or
simply by working with fish. Undoubted ly, the
most commonly disseminated are microbial
pathogens which can cause a various range of
infections and intoxications in humans.
The restrictions applied during the Stockholm
Convention, have partly achieved to eliminate
the use of numerous hazardous chemically
3
synthetized solutions. Still, pesticides are
available on the black market in less developed
and developing countries (Carpenter, 2011) . The
lack of environmental education encourages
oblivious people to continue spraying or even
dumping such substances. The infections with
pathogenic bacteria are usually accidental, a
consequence of a hygiene deficiency or
insufficient thermal treatment. Global pollution
is making a statement regarding this aspect as
well. Microbe s are multiplying easier than
before, they are more resistant and more
aggressive.
The objectives of this paper are to describe the
most important chemical and bacterial causative
agents of human diseases in fish meat, the
frequency and the way in which hu mans can be
exposed to these factors and eventually their
toxic effects, in order to increase public
awareness concerning the consumption and
handling of fish and fish products in the context
of European residue monitoring.
CHEMICAL CONTAMINANT S
TYPES OF POPs IN FISH MEAT
The classification of POPs includes groups like
organochlorine compounds (OCs),
polybrominated diphenyl ethers (PBDEs),
PCBs, dioxins and furans. From these groups,
the dioxin and furans are the only substances
that humans didn’t create t hemselves, but
appeared when burning chlorinated solutions at
low temperatures.
From the group of OCs, some compounds
usually stand out more in research studies, but
also in the day by day discussions of people with
other professions. A very popular chemic al
contaminant is dichlorodiphenyltrichloroethane
(DDT), known to be very effective against
mosquitos and intensively used in low
developed countries in order to prevent malaria
(Carpenter, 2011) . DDT is closely followed by
gamma-hexachlorocyclohexane (Lindane),
Aldrin, Dieldrin. The list could definitely
continue with numerous less known substances
which still have an important ongoing impact in
our environment, however some clear examples
found in samples collected from humans are
better described in Table 1 . WAYS OF EXPOSURE
Directly, people can be more aggressively
exposed to chemical contaminants (e.g.
insecticides, fungicides) as an outcome of
occupational, agricultural and household use.
Occupational exposure can generate Parkinson
disease, all forms of haemapoethic cancers,
breast cancer in women, bladder cancer,
meningioma (Kim et al., 2016) .
Crops spraying with pesticides by people that
have not received a proper training in this type
of activity, who cannot safely handle the
solutions and do not know how to protect their
selves, can cause symptoms such as nausea or
vomiting , headaches, blurre d vision and eye
irritation , but also respiratory problems (Sankoh
et al., 2016, Sumon et al., 2016).
Inhaling, skin -to-skin contact, accidentally
drinking or exposing the eyes to vapours can
cause acute symptoms with hazardous
consequences that could eve n lead to death. If
the concentration and the toxicity are high, the
risks are proportionally higher (Sabra and
Mehana, 2015) . If the person lives after the
direct exposure, after causing the intended
damage of the organism, PO Ps can be again
released in the environment through urine, sweat
or exhaled hair.
Indirectly, POP residues can be transmitted to
humans through daily food intake , fish meat
being a very good vector due to its capacity of
accumulating residues from water, s ediments,
and feed .
Samples taken from I nuit people have revealed
high amounts of POP residues. The specific diet
consisting in plenty of fish and fats is the way in
which chemical contaminants easily entered the
human body, behaving as markers of
inflamm ation which might later provoke
rheumatoi d arthritis, atherosclerosis or hence
cardiovascular disease (Schæbel et al. 2017; Wu
et al. 2016).
Another recently discovered path that POPs use
to find their way in is the ingestion of
contaminated supplements ba sed on fish oil. The
primary goal of these supplements was to
improve human hea lth. Hong, 2015 showed in
his study conducted on rats, that if POP residues
4
Table 1 POPs monitoring in human subjects
Country Studied POPs Most frequently detected
compounds Sample
type Survey period Age of
donors Conclusions References
Australia (South
East Queensland) hexachlorobenzene (HCB), β –
hexachlorocyclohexane
(β-HCH), γ –
hexachlorocyclohexane
(lindane) (γ –
HCH), oxy -chlordane, trans –
nonachlor, p,p′ -DDE, o,p′ –
DDT, p,p′ -DDT, Mirex HCB, β -HCH, trans –
nonachlor, p,p′ -DDT and
p,p′-DDE Serum 2002/03
2006/07
2008/09
2010/11
2012/13 All ages Females had higher levels of POPs than men
(especially in the elder category) . (Thomas et al.,
2017)
U.S.A 13 organochlorine compounds
(OCs), 10 polybrominated
diphenyl ethers (PBDEs),
polybrominated biphenyl (PBB)
153, 38 polychlorinated
biphenyls (PCBs), 17
polychlorinated
dibenzo -p-dioxins and
dibenzofurans (PCDDs/Fs), 12
perfluorinated compounds
(PFCs) – Blood 2003/04 ≥ 20 years
old More than 13% of the U . S. A. population may have
10 POPs each at concentrations in the top decile . (Pumarega et al.,
2016)
Tanzania (Arusha) HCB, α -HCH, β -HCH, γ -HCH,
ΣHCH, Oxychlordane, cis –
Chlordane, trans -Nonachlor,
ΣCHL, p,p′ -DDE, p,p′ -DDD,
p,p′-DDT,, ΣDDTs
Dieldrin, Endosulfan I,
Endosulfan sulfate,,
ΣEndosulfan, PCB−28,
PCB−52, PCB−101, PCB−118,
PCB−138, PCB−153,
PCB−180, Σ6PCBs , Σ7PCBs Dichlorodiphenyltrichlor
oethane (DDT) and its
metabolites, dieldrin,
PCB−153 Milk – 19–24,
25–30 The main findings were the wide -ranging
concentrations of DDTs and dieldrin ;
Despite the occurrence of potential harmful chemicals
in the Tanzanian breast mil k, mothers should been
encouraged to breastfeed their infants, as the
nutritional, immunologic and developmental benefits
from breastfeeding may outweigh the possible
negative effects from chemical exposure . (Müller et al.,
2017)
Russia (Eastern
Siberia) HCB, α -HCH, γ -HCH, ΣHCH,
α /γ -HCH, p,p’ -DDE, p,p’ –
DDD, p,p’ -DDT, ΣDDT,
DDE/DDT PCB -28, PCB -52,
PCB -101/90, PCB -153, PCB –
138, PCB -180, ΣPCB 6, ΣPCB 26 DDTs > PCB > HCB >
HCHs Milk – – A relatively homogeneous contamination across
almost the whole region;
The population of Irkutsk Region undergoes both
environmental and occupational exposure to POPs . (Mamontova et al.,
2017)
Croatia (Zadar) PCB -28, PCB -52, PCB -101,
PCB -138, PCB –
153, PCB -180 (six indica tor
congeners), PCB -77, PCB -126,
PCB -169 (three non -ortho
congeners), PCB -105, PCB –
114, PCB -118, PCB -123, PCB –
156, PCB -157, PCB -167, PCB –
189 (eight mono -ortho
congeners), PCB -60, PCB -74 ΣPCBs > ΣDDTs >
ΣHCHs > HCB Milk 2011 24-45 Levels were lower in samples from multiparae than in
primiparae samples ;
POPs found in this study should not raise concern for
mothers or breastfed infants . (Klinčić et al.,
2016)
5
and PCB -170,
hexachlorobenzene (HCB), α -,
β-, γ –hexachlorocyclohexan es
(α-HCH, β -HCH, γ -HCH), 1,1 –
dichloro -2,2-di(4-
chlorophenyl)ethylene (p,p´ –
DDE), 1,1 -dichloro -2,2-di(4-
chlorophenyl)ethane (p,p´ –
DDD), and 1,1,1 -trichloro -2,2-
di(4-chlorophenyl)ethane (p,p´ –
DDT)
Croatia (Zadar,
Zagreb) α-HCH, HCB, β -HCH
γ –HCH, p,p’ -DDE, p,p’ -DDD,
p,p’-DDT, PCB -28, PCB -52,
PCB -74, PCB -60, PCB -101,
PCB -77, PCB -123, PCB -118,
PCB -114
PCB -153, PCB -105, PCB -138,
PCB -126, PCB -167, PCB -156,
PCB -157, PCB -180, PCB -169,
PCB -189 α-HCH, HCB, β -HCH, γ –
HCH, p,p’ -DDE, p,p’ –
DDT, PCB -60, PC B-101,
PCB -123, PCB -118,
PCB -105 , PCB -156,
PCB -157, PCB -28, PCB –
52, PCB -153, PCB -138,
PCB -180, PCB -170 Milk 2009/10,
2009/11 22-37
20-33 PCB and OCP were found to be in the lower part of the
concentration ranges found in other European
countries;
Clear decreasing trend of organochlorine levels in the
human milk samples collected from donors living in
Zagreb during a10 -year period;
The most toxic PCB congeners were not found in any
of the samples. (Klinčić et al.,
2014)
Poland (central
Poland) PCB -81, PCB -77, PCB -123,
PCB -118, PCB -114, PCB -105,
PCB -126, PCB -167, PCB -156,
PCB -157, PCB -169, PCB -189 Milk 2008/10 23-24
22-38 The median concentration of PCDD/Fs and dl -PCBs
found in breast milk samples (n = 40) from the Polish
mothe rs (5.8 – rural and 7.7 pg. WHO TEQ/g fat in
urban area) is one of the lowest in comparison with
other European countries (Kamińska, 2014)
Saudi Arabia
(Eastern district of
Saudi Arabia) p,p’-DDD, p,p’ -DDE, p,p’ –
DDT, ΣDDT, Dieldrin,
ΣDieldrin, Lindane, Heptachlor
epoxides p,p’-DDE, p,p’ -DDD,
Lindane (γ -HCH),
Dieldrin,
Endrin, A -heptachlor Milk – 18-30 DDE, DDD and HCH were the main contributors to
the total OCs detected in human milk;
The concentrations of OCs residue found in mothers'
milk from the study area were generally far below the
MRL;
Risk assessment for infants weight 3.5 kg and ingest
750 ml of human milk daily, presented that the EDIs
of total DDT and Lindane ingested daily by infant feed
on mother milk were far below the ADI
standard issued by European Food Safety Authority;
The EDI of Dieldrin and Heptachlor, for infant, were
higher than the ADI standard accepted by EU. (Hajjar and Al –
Salam, 2016)
Spain (Almeria) Abamectin, Tebuconaz ole ,
Azadirachtin,
Acetamiprid, Spinosad,
Cyprodinil, Fludioxonil,
Myclobutanil, Chlorthalonil,
Fluopicolide, Propamocarb,
Copper oxychloride,
Spiromesifen, Mepanipyrim
Pyrimethanil, Methomyl,
Bacillus thuringiensis,
Dimethomorph, Azoxystrobin,
Thiophana te methyl, – Blood 2011 18-66 Chronic occupational exposure to pesticides of lower
toxicity elicit mild toxic effects, particularly targeting
the skin and eyes, as well as subtle subclinical
(biochemical) changes of unknown long -term
consequences. (García -García et
al., 2015)
6
Imidacloprid, Indoxacarb,
Cypermethrin, Deltamethrin
Brazil (Rio
Branco) α-HCH, β -HCH, γ -HCH
(lindane), HCB, Heptachlor,
Heptachlor epoxide, Heptachlor
epoxide, α -Chlordane, γ –
Chlordane, trans, Nonachlor,
p,p′-DDT, o,p′ -DDT, p,p′ -DDE,
o,p′-DDE, p,p′ -DDD, o,p′ –
DDD, Endosulfan, Endosulfan,
Aldrin, Endrin, Dieldrin, Mirex,
Methoxychlor,
Pentachloroanisole, DDT/DDE
ratio p,p′-
dichlorodiphenylethane
(p,p′-DDE), lindane (γ –
hexachlorocyclohexane),
hepta chlor, p,p′ –
dichlorodiphenyltrichlor
oethane (p,p′ -DDT) Blood 2010/11 18-30
30-49
50-65 The observed occurrence of p,p′ -DDE (32%) and
lindane (20%), andthe low DDT/DDE ratio, may
indicate higher historical exposure to theinsecticides
DDT and lindane in this population relative to other
OC pesticides;
Exposure to OC pesticides in Rio Branco, Acre, seems
to be low. (Freire et al.,
2017)
Tunisia (Bizerte) HCB 25, α -HCH, β -HCH, γ –
HCH, δ -HCH,
HCHs, α -HCH/β -HCH, α –
HCH/γ -HCH, o,p′ -DDE, p,p′-
DDE, o,p′ -DDD, p,p′ -DDD,
o,p′-DDT, DDTs, p,p′ –
DDT/p,p′ -DDE, OCPs, PCB 18,
PCB 28/31, PCB 52, PCB 44,
PCB 101, PCB 149, PCB 118,
PCB 153, PCB 138, PCB 180,
PCB 170, PCB 194, PCBs p,p′-DDE, p,p′ -DDT,
HCB and β -HCH;
DDTs>PCBs>HCB>HC
Hs Adipose
tissue – 20-85 Fish consumption may be an important contributor of
PCBs adipose tissue con tent of PCBs in Tunisian
people;
Continuous source of illegal use of DDT and
decreasing trend in thelevels of exposure of HCB,
HCHs and PCBs;
A lack of age -dependent increase in concentrations of
all studied OCs for men;
The trend of increasingHCB, DDTs and PCB 118
concentrations with increasing age were observed for
women . (Achoura et al.,
2017)
7
are present in supplements containing fish oil,
then the supplements can cause the negative
effects on antioxidant capacity and lipid
peroxidation processes (Alewu et al., 2011) .
EFFECTS IN FISH
Some of the effects of POPs in animal
organisms can give information about their
possible action in the human body. For this,
studies use fish collected from their natural
environment or fish as experimental animals.
The biomonitoring of especially edible fish is
important (Ferna ndes et al., 2015) .
Berg et al., 2016 revealed that chemical
contaminated fish showed symptoms of
endocrine disruption (changes in the adrenal
and gonadal axis parameters). Some
physiological functions like reproduction and
weight homeostasis were neg atively
influenced as well (Berg et al., 2016) .
Oxidative damage in tissues, a higher number
of white blood cells and low liver transaminase
activity are possible with Endosulfan
combined with lambda -cyhalothrin
(Bacchetta, 2016) . Other signs present in fish
were developmental anomalies and lethal or
sublethal effects (Mensah et al. 2014; Murthy
et al. 2015).
Fish liver is one of the most susceptible organs
to POPs, but there are other locations possible
inside the body where POPs can be discovered
or where they raise disorders (e.g. kidney,
brain).
EFFECTS IN HUMAN HEALTH
Women are more susceptible to some POPs
(e.g. PCBs) than men (Wu et al., 2016) .
Although t he most dangerous effect of POPs is
manifested in pregnant women, babies and
small children. These are the most sensitive
categories, which captivated the attention of
researches from all over the world. The
ingestion of chemical contaminated fish can
affect the r eproductive capacity but also
neurobehavioral development, especially
when DDTs or mixtures of substances are
involved. Numerous recommendations with
safer foods from this perspective, are placed as
an alternative for fish in expecting women
diets and some times, even avoiding or not
consuming fish at all is considered proper (Binnington et al., 2014) . Fat fish such as
salmon, tuna and crustaceans, but also other
seafood (e.g. eel) coming from polluted areas
should be especially kep t away from pregnant
women due to their capacity to accumulate
large amounts of lipophilic POPs (van den
Dungen, 2016; Mendez et al. 2009; Mori and
Todaka, 2017).
Children who are still developing are more
susceptible to the effects of chemical
contaminan ts. Substances such as PCBs can
interfere with their metabolic health (Lee et al.,
2016) , while others can cause dreadful
illnesses (e.g. lymphoma, leukemia) (Kim et
al., 2016; Wu et al., 2016). Also, children who
were exposed before being born are linked to
more reduced IQs, inability to focus or cope
with frustration (Carpenter, 2011) . In adults,
the cognitive tests revealed an increased
cognitive impairment risk for men and women
with higher levels of POPs in their bodies (Kim
et al., 2016) .
Depending on their chemical structure, similar
POPs have can alt er human health through
identically or at least very much related. Some
like OCs act more as initiators of chronic
disease, while others like dioxins and PCBs
can add being even cancers -causing factors
(Kim et al, 2016; WHO, 2016, Wu et al. 2016) .
Contrary to ω-3 fatty acids’ ability to prevent
cancer build -up, a melanoma analysis
conducted on people that have been eating
chemical contami nated fish from a lake in
U.S.A. for many years, suggested a high
incidence of melanoma (Green, 2 015)
Carpenter, 2011 and Gascon et al. 2013 state
that early exposure to POPs can have
repercussions on the immune system making
not only animals die from immunosuppression,
but also children to become more sensitive to
respiratory diseases.
In the la st decade, the interest in whether POPs
are being involved or not in obesity and
diabetes grew. A rich diet in fatty fish such as
salmon was demonstrated to contribute in the
development of insulin resistance which leads
to diabetes type 2 (Carpenter, 2011 ; Ibrahim et
al., 2011; Kim et al., 2016; Marushka et al.,
2017; Turyk et al. 2015). Eating fat
automatically increases the chances of obesity
for which POPs appear to be a providing factor
8
(Le Magueresse -Battistoni et al., 2014) . Trying
to lose weight in such cases can convert into an
issue also. Rapid weight loss can set free POP
residues which were previously held in the
adipose tissue, directly into the bloodstream
(Lee et al, 2017; Rouhou et al, 2016). From
blood, POPs can reach any organ or system in
the body. Adverse effects of weight loss can be
correlated with this flow, but more studies
have to be performed in this way in order to
demonstrate it.
MYCROBIOLOGICAL
CONTAMINANTS
THE BACTERIAL MICROFLORA OF
FISH
Different studies have been indicated that fish
contain bacterial populations on or in their
skin, digestive tract, gills, muscles (Austin,
2002) . Mostly, the area of bacterial species
isolated is associated with marine environment
of the fish, and fluctuates with various factors
such as season, salinity of the habitat, feeding
type, etc. (Gonzalez et al., 2001) . Due to the
contaminated water, bacterial colonization can
be observed on gills and skin surface, bei ng
generally accepted that bacteria found on fish
skin are the same as the ones found in the
pollute water, including species as Aeromonas
spp ( Aeromonas hydrophila, A. bestiarum, A.
caviae, A. jandaei, A. veronii) , Proteus spp,
Moraxella spp, Pseudomon a flourescens,
Enterobacter aer ogenes, Micrococus luteus,
Vibrio fluvialis, Flexibacter spp, Providencia
spp. (González -Rodríguez , 2002) The gill
microflora is being mostly populated by
Achromobacter, Baccilus, Flavobacterium and
Micrococcus.
The contamination of digestive tract and fish
muscles is put on the record thanks to
contaminated feed and water, plus the failure
of immunological resistance (Mar ı́a Cecilia
Guzmán, 2004) .
Normally, the internal organs (kidney, liver,
spleen) and muscles of healthy fish are germ –
free, although recent studies have described the
presence of bacteria ( Pseudomonas spp, Vibrio
spp including V. fischeri, V. p elagius) , and there is discuss either the fish muscle is ster ile
or not ( Evelyn and McDermott, 1961) .
Microflora of fish guts, appears to differ with
the complexity of fish gastrointestinal tract, the
type of fish feed; the species present in the
intestines seem to be those from the
environment and the higher bacterial culture
was found in detritus eaters (Balasubramanian
et al., 1992) .
An extensive range of taxa have been
correlated with the digestive tract of fish and
contain Aeromonas spp, Alteromonas spp,
Flavobacterium spp, Pseudomonas spp,
Staphylococcus spp, Escherichia spp,
Klebsiella spp, Proteus, Serratia,
Mycoplasma, and Vibrio spp (Kim DH, 2007) .
According to European Food Safety Authority
(EFSA), a wide range of bacteria such
Campylobacter, Listeria, Salmonella, E. coli
can be responsible for foodborne outbreaks,
threatening public health directly (EFSA,
2014) . Nonethe less, not all the pathogens are
incriminated in the foodborne outbreaks
considering the consumption of fish and fish
products, however, some bacterial species like
Listeria monocytogenes, E. coli, Vibrio spp,
Salmonella spp, C. botulinum , Streptococcus
iniae, Mycobacterium spp, present a lot of
interest, due to their ample dispersion in the
marine environment, and also to the high
morbidity and mortality rates for human
beings.
FOODBORNE PATHOGENS RELATED
WITH FISH AND FISH PRODUCTS
Mycobacterium spp
Mycobacteria are a class of rod -shaped
bacteria, acid fast, that do not stain by
traditional methods, for this species procedures
such as Ziehl -Nielsen staining and biopsy are
necessary in order to isolate and detect them
(Beran et a l., 2006) .
Mycobacteria are the most known zoonotic
fish-borne bacterial germs, affecting a large
range of fish species worldwide, being
responsible for the affection called
mycobacteriosis ( fish tuberculosis) (Novotny
et al., 2 004), a chronic progressive disease,
causing granulomatous inflammation, in
9
viscera and muscles, as well as ulcerative skin
lesions (Gauthier, 2009) . Injuries tend to be
observed two to four weeks after exposure to
the myco bacterium. Usually disease in humans
appear as superficial granulomatous
inflammation of the extremities because of the
cooler temperatures, and in some instances
long term effects involve deeper tissues,
resulting tenosynovitis, osteomyelitis, arthritis
and a non -responsive immune system. (Petrini,
2006) . The most commonly detected species
involve: M. marinum, M. fortuitum, M.
chelonae. The human population contact fish
pathogenic mycobacteria, due to exposure of
wounds and skin abrasion to polluted water, as
well as injuries contracted by handling infected
fish or bye seefood preparation and processing.
(Rhodes e t al., 2004) . The diagnosis is difficult
based on the ability of mycobacterium
(particularly M. marinum) to mimic other
disorders such as gout, chronic infections,
rheumatoid arthritis. Infections with M.
marinum are clinicaly and histologically
indis tinguishable from tuberculosis.
Moreover to their direct effects, M. marinum
and other non -tuberculous mycobacteria
(NTM) can lead to cross – reactivity to skin
tests based on purified protein derivative
(PPD) of M. tuberculosis and M. avium
(Kobashi et al., 2009) . Antibiotic theraphy is
necessary, to treat the skin condition, in deep
lesions the surgical excision is often
indispensable. (Lewis et al., 2003) .
Clostridium botulinum
Clostridium botulinum is being of the genus
Clostridium, is a spore forming bacteria,
associated with foodborne botulism that grows
at anaerobic conditions. (Novoslavskij et al.,
2015) . The main habitat of this germ is wide
spread in nature , from soil ground to marine
environments. Virulence of the bacteria consist
in producing a neurotoxin that causes botulism,
a disease which attacks the central nervous
system causing descending paralysis in
humans (Barash and Amon, 2014) . There are
seven t ypes of toxins developed by C.
botulinum, type E being involved mostly in
cases of human disease linked with fish
consumption (Lindström et al., 2006) Sometimes type A and B also involved
(Hyyatia , 1998) . The existence of C.
botulinum in fish can be related to direct
contact with polluted water environments and
ingestion of C. botulinum spores from
sediments and contaminated feed (Leclair et
al., 2006) . Clostridium botulinum can pose a
threat to public health when processing
technics are improper and insufficient to
eliminate botulinum spores from raw fish.
Enterobacteriaceae
Enterobacteriaceae are ubiquitously
distributed in a wid ely range of environments
and hosts, and a various number of pathogenic
species have been isolated from fishes,
including entheropathogenic E. Coli and
Salmonella spp , bacterial causative agents of
gastroenteritis in humans. (EFSA, 2 014)
The contamination of fish with pathogenic E.
coli possibly occurs by handling of fish or
during the production proces s (McCoy et al.,
2011) . Some outbreaks concerning E. coli have
been described in Brazil where authors have
isolated 18 enterotoxigenic strains of E. coli
(ETEC) from fresh fish, from Brazilian
markets (Vieira et al., 2001) ;
enterohaemoragic strain (EHEC) of E. coli
from salted salmon roe in Japan. (Asai et al.,
1999) Some strains Shiga -toxin producers are
capable to cause foodborne diseases.
Salmonella is a mesophilic organism and is not
a usual inhabitant of water environments
(Kumar et al., 2009) . The bacteria presence in
aquatic climate is mainly explained by hygiene
failures during production (Amagliani et al.,
2012) . Salmonella can be isolated from fresh
water, not just from seafood; this thing being
explained by contamination of water source.
Salmonella can be divided in more than 2500
serovars. (Agbaje et al, 2011)
Nonetheless some serovars are desc ribed as
being major dominants in fish meat and aquatic
habitats, such Salmonella enterica ser.
Bareilly, ser. Ohio, ser. Newport, ser. Derby,
ser. Tyiphimurium, ser. Washington etc. Other
salmonella including Salmonella enterica ser.
Enteritidis, ser. Typ hi, ser. Paratyphi B , were
mentioned as co mmon serotypes isolated from
seafood (Rahimi et al., 2013) . In conclusion,
10
the prevalence of E. coli and Salmonella
serovars in fish and water environments is a
widespread concern in foo d handling and poor
hygiene during the capture, transport, and
processing of fish.
Vibrio spp
Vibrio spp are widely distributed in estuary
waters and fish habitats (Feldhusen, 2000) . A
variety of fish pathogenic species can cause
diseases including Vibrio anguillarum the
causative agent of red pest in eels, V. ordalii
causes septicaemia in salmonids, V.
salmonicida causes cold water vibriosis, V.
vulnificus causes warm water vibriosi s, V.
wodanis causes winter ulcer disease in Atlantic
salmon (Gauthier, 2014) . Among Vibrio spp ,
that cause diseases in humans the most
significant is V. cholerae , particularly the toxin
strains that belong to O1 serogroup, ho wever
V. cholerae is hardly reported as a disease
agent in fishes. The non -cholera human
vibriosis are caused by V. parahaemolyticus
and V. vulnificus (Gauthier, 2014) . V.
vulnificus is a gram -negative pathogen,
causing gastroe nteritis or septicaemia in
humans after ingesting raw seafood. There are
three biotypes described for this species;
biotype 1 is isolated from water and humans,
biotype 2 is isolated from humans and fishes,
biotype 3 has been isolated from humans and
woun d infections and is supposed to be a
hybrid between biotypes 1 and 2 (Mahmud et
al., 2010) . V. parahaemolyticus is the author of
acute gastroenteritis, on rare occasions
septicaemia can occur; being frequently
isolated from fish, mollusks and crustaceans.
These pathogens can cause human vibriosis,
due to consumption of insufficiently heat –
treated fish or fish produ cts (Callol et al.,
2015) .
Streptococcus iniae
Streptococcus iniae is a Gram -positive,
encapsulated coccus, that causes
meningoencephalitis and high losses in finfish
aquacultures (Agnew and Barnes, 2007) .
Streptococcus iniae was first reported in 1976
as the causative agent of “golf ball disease”, a
disorder defined by multiple subcutaneous abscesses in Amazon freshwater dolphins.
Humans tend to develop a bacteraemic
cellulitis developed in 16 -24h a fter a
percutanaeous injury (Facklam, 2005) while
preparing fish for consumption, zoonotic risk
seem to be correlated with older and
immunocompromised people (Locke et al.,
2007) . In fish the infection results in a
meningitis and panophthalmitis, and a high
rate of morbidity and mortality. Clinical signs
may include: exophthalmia, melanosis, corneal
opacity, loss of orientation, emaciation or
sudden death (Evans et al., 2008) . Fish may get
infected by diverse routes of exposure like
oral, olfactive route, direct contact, or through
cannibalism. Diagnosis in fish should be
pronounced as a result of combination between
clinical signs, etiological isolation , pathology
findings.
Listeria monocytogenes
Listeria monocytogenes is a pathogenic agent
widespread in nature, can be found in soil,
silage, fresh and marine waters, sediments. Is
the causative agent of listeriosis in human
beings (Liu, 2006) . The prevalence of listeria
is correlated with the degree of human activity.
There are more than 13 serotypes described for
L. monocytogenes , on which certain serotypes
(1/2a, 1/2b and 4b) are involved in human
cases (Jami et al., 2014) ; these serotypes are
found mostly in fish too. Listeria
monocytogenes and other species, persist in
water climate due to their abilities to survive
and multiply at low temperatures (40C) and by
forming biofilms (Budzińska et al., 2012) .
Listeria has been found in processed seafood
products, marinated fish, sushi, smoked fish
(Tocmo et al., 2014) . A low number of
listeriosis epidemic episodes have been relat ed
with the consumption of fish or fish products
in analogy with other foods (EFSA, 2014) .
Bacterial pathogens can contaminate the fish
products during the processing technology.
Evisceration and scalding of the fish before
mark eting can lead to cross -contamination of
fish, utensils, personnel, surroundings.
Cleaning and sanitation programs were
recommended to avoid contamination with L.
Monocytogenes on the surfaces and equipment
11
during the processing time (Papadopoulos et
al., 2010) .
CONCLUSIONS
A wide range of chemical contaminants and
microbes in fish and seafood have been
described as potential risks for foodborne
outbreaks .
Factors such as human activity, hygiene
deficits during handling, transport and
processing technologies, cont aminated water
and air have an important impact for the
development of acute and chronic symptoms
from POPs and bacteria in humans.
In the case of chemical contaminants, risks can
be av oided more through the consumption of
less fatty fish, avoiding to eat fish and seafood
in case of pregnancy or to offer it to small
children who are still in development phase.
The emergence of bacterial microorganisms is
based on outbreaks deriving from the
consumption of raw or insufficient cooked fish
meat. Therefore, a more careful approach
towards this could be efficient.
Guidelines such as Good H ygiene Practices
(GHP) together with Good Manufacturing
Practices (GMP) and the implementation of a
Hazard Analysis and Critical Control Point
(HACCP ) program for fish, fish products and
seafood, are some measures that could lower
the risks of foodborne diseases.
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