Comp Rev Food Sci Food Safe - 2020 - Sheng

Received: 2 July 2020 Revised: 22 September 2020 Accepted: 12 October 2020
DOI: 10.1111/1541-4337.12671
COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY
The microbial safety of fish and fish products: Recent

advances in understanding its significance, contamination
sources, and control strategies
Lina Sheng Luxin Wang
Department of Food Science and

Technology, University of California, Abstract
Davis, Davis, California, USA Microorganisms play a crucial and unique role in fish and fish product safety. The
Correspondence
presence of human pathogens and the formation of histamine caused by spoilage
Luxin Wang, Department of Food Science bacteria make the control of both pathogenic and spoilage microorganisms crit-
and Technology, University of California, ical for fish product safety. To provide a comprehensive and updated overview
Davis, 1136 RMI North, Davis, CA 95616.
Email: lxwang@ucdavis.edu of the involvement of microorganisms in fish and fish product safety, this paper
reviewed outbreak and recall surveillance data obtained from government agen-
cies from 1998 to 2018 and identified major safety concerns associated with both
domestic and imported fish products. The review also summarized all available
literature about the prevalence of major and emerging microbial safety concerns,
including Salmonella spp., Listeria monocytogenes, and Aeromonas hydrophila,
in different fish and fish products and the survival of these pathogens under dif-
ferent storage conditions. The prevalence of antibiotic-resistant bacteria (ARB)
and antibiotic-resistant genes (ARGs), two emerging food safety concerns, is also
reviewed. Pathogenic and spoilage microorganisms as well as ARB and ARGs
can be introduced into fish and fish products in both preharvest and postharvest
stages. Many novel intervention strategies have been proposed and tested for the
control of different microorganisms on fish and fish products. One key question
that needs to be considered when developing and implementing novel control
measures is how to ensure that the measures are cost and environment friendly
as well as sustainable. Over the years, regulations have been established to pro-
vide guidance documents for good farming and processing practices. To be more
prepared for the globalization of the food chain, harmonization of regulations is
still needed.
KEYWORDS
antimicrobial resistant, contamination sources, fish safety, interventions, microbiome,
pathogens
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the
original work is properly cited.
© 2020 The Authors. Comprehensive Reviews in Food Science and Food Safety published by Wiley Periodicals LLC on behalf of Institute of Food Technologists
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MICROBIAL SAFETY OF FISH AND FISH PRODUCTS. . . 739
1 INTRODUCTION 2015; Novoslavskij et al., 2016). It is well accepted

that microorganisms are commonly present on fish sur-
According to the Food and Agriculture Organization faces, such as skin and gills, as well as inside of the
(FAO) (2020), world fish production has increased dra- fish in areas such as the digestive tract and internal
matically during the past 60 years, to around 179 million organs, for example, the kidney, liver, and spleen. How-
tons in 2018 with a value of $401 billion. Global fish con- ever, fish and fish products, especially raw or under-
sumption also increased from 9.0 kg per capita in 1961 to cooked products, have been involved in outbreaks asso-
20.5 kg in 2018. Aquaculture production presents 46% of ciated with bacterial pathogens, biotoxins, histamine,
the total production and 62% of the total sale value. Due to viruses, and/or parasites (Galaviz-Silva, Goméz-Anduro,
the increasing demand for high-quality protein, reduction Molina-Garza, & Ascencio-Valle, 2009). Fish have been
of the wild fish catch, and advancement in fish farming identified as reservoirs of bacterial pathogens linked to
technologies, global aquaculture production is expected to human diseases including Mycobacterium spp., Streptococ-
double by 2050 (Ibrahim et al., 2020). China is the major cus iniae, Photobacterium damselae, Vibrio alginolyticus,
producer of aquaculture fish, contributing more than half Vibrio vulnificus, Vibrio parahaemolyticus, Vibrio cholerae,
of the global production. Carp, tilapia, and salmon are Erysipelothrix rhusiopathiae, pathogenic Escherichia coli,
the top three finfish species produced globally. According Aeromonas spp., Salmonella spp., Staphylococcus aureus,
to the United States National Oceanic and Atmospheric Listeria monocytogenes, Clostridium botulinum, Clostrid-
Administration (NOAA) (2020), in 2017 the United States ium perfringens, Campylobacter jejuni, Delftia acidovo-
ranked 17th in aquaculture production with an estimated rans, Edwardsiella tarda, Legionella pneumophila, and
625.7 million pounds valued at $1.47 billion. The leading Plesiomonas shigelloides (Novotny, Dvorska, Lorencova,
species for freshwater and saltwater production are catfish Beran, & Pavlik, 2004). In addition, the presence of
(330.4 million pounds) and Atlantic salmon (32.4 million antibiotic-resistant genes (ARGs) in these microorgan-
pounds), respectively. The United States has also been the isms has caused concerns about spreading antibiotic resis-
leading importer of fishery commodities, in 2018 import- tance (AMR) in the environment and to human beings
ing 6.1 billion pounds of edible fishery products valued at (Brunton et al., 2019; Preena, Swaminathan, Kumar, &
$22.4 billion. Singh, 2020; Watts, Schreier, Lanska, & Hale, 2017). In
Based on the U.S. Food and Drug Administration (FDA) addition to human pathogens, bacteria are considered
Code of Federal Regulations Title 21 (21CFR), fish is the primary cause of fish spoilage (Rippen & Skonberg,
defined as freshwater and saltwater finfish, crustaceans, 2012). Certain spoilage bacteria can produce decarboxy-
mollusks, and other forms of aquatic animal intended for lase enzymes and convert free histidine to appreciable
human consumption (21CFR123.3). Fish products repre- quantities of histamine, resulting in scombroid poison-
sent any human food product containing fish as a charac- ing, another food safety concern (Colombo, Cattaneo, Con-
terizing ingredient (21CFR123.3). In 2018, 2,221 fish species falonieri, & Bernardi, 2018).
were captured, 622 of which belong to aquaculture produc- Pathogenic and spoilage microorganisms can be intro-
tion (FAO, 2020). About 88% of the global fish production duced into fish and fish products at any point throughout
are for direct human consumption, 44% of them are in live, the production and supply chain. The application of next-
fresh, or chilled statuses, forms that are most preferred and generation sequencing (NGS) technologies has allowed
highly priced in many markets (FAO, 2020). The rest of in-depth insights into the fish microbiome—the consor-
production is processed, with 35% frozen, 11% in prepared tium of all microbial habitants in fish and the surround-
and preserved forms, and 10% dried, salted, smoked, or oth- ing environment—which facilitates better understanding
erwise cured (FAO, 2020). Because finfish contributes to of the sources of pathogenic and spoilage microorgan-
more than 65% of world food fish production, the fish and isms (Brugman et al., 2018; Legrand, Wynne, Weyrich,
fish products discussed in this review paper refer to fin- & Oxley, 2019; Marchesi & Ravel, 2015; Ross, Hoffmann,
fish and finfish products. In the United States, 76.5% of & Neufeld, 2019; Tan et al., 2019; Yukgehnaish et al.,
domestic landings were consumed fresh and frozen, 1.9% 2020). Understanding the prevalence, ecology, concentra-
canned, and 1.5% cured (NOAA, 2020). The top processed tion, and dynamics of pathogenic and spoilage microor-
fish species in 2018 were Alaska pollock (1.6 billion pounds, ganisms present throughout the entire fish production
$1.98 billion), sockeye salmon (193 million pounds, $940 chain will also contribute to the development and appli-
million), tuna (384 million pounds, $836 million), and cod cation of new intervention strategies. Various decontam-
(292 million pounds, $745 million). ination methods have been proposed, tested, and applied
Fish is considered a safe food in general, and the to ensure the microbiological safety of fish and fish prod-
muscles of healthy fish are considered sterile, although ucts, including physical, chemical, and biological inter-
debate on this continues (Austin, 2006; Karunasagar, ventions (da Cunha, Heinzmann, & Baldisserotto, 2018;
740 MICROBIAL SAFETY OF FISH AND FISH PRODUCTS. . .
Kuebutornye et al., 2020; Kumar, Mukherjee, & Dutta, T A B L E 1 The numbers of fish-associated outbreaks and their
2020; Ringø et al., 2018; Sternisa, Mraz, & Mozina, 2016). percentages in the total foodborne outbreaks in the United States,
Advancements in these areas, for example, photodynamic 1998 to 2018
inactivation of bacteria and the identification of new nat- Total fish- Confirmed
ural antimicrobials, warrant further investigation as tech- associated fish-associated
niques to ensure fish and fish product safety. outbreaksa outbreaksb
This review aims to provide updated information about Year No. (%) No. (%)
outbreaks and recalls associated with fish and fish prod- 2018 45 (4.3) 39 (8.2)
ucts in the past 25 years, identify major microbial con- 2017 37 (4.4) 32 (7.9)
cerns associated with fish products, and evaluate the pres- 2016 26 (3.1) 24 (5.8)
ence and prevalence of AMR in fish and fish products. 2015 34 (3.7) 30 (6.6)
Furthermore, the survivability of major and emerging 2014 44 (5.0) 39 (8.2)
human pathogens on fish products under different stor- 2013 50 (6.0) 33 (7.3)
age conditions and sources that contribute to final micro- 2012 31 (3.7) 24 (5.6)
bial abundance and diversity on fish and fish products is
2011 30 (3.8) 24 (6.4)
reviewed. Accordingly, recent development and optimiza-
2010 17 (2.0) 13 (2.8)
tions of intervention strategies that can be applied during
2009 18 (2.7) 16 (4.5)
both pre- and postharvest stages are summarized.
2008 29 (2.8) 24 (5.0)
2007 41 (3.7) 30 (5.9)
2 MICROBIOLOGICAL SAFETY OF 2006 48 (3.8) 42 (6.8)
FISH AND FISH PRODUCTS 2005 43 (4.5) 40 (9.8)
2004 52 (3.9) 44 (8.1)
2.1 Outbreaks and recalls 2003 68 (6.2) 50 (11.9)
2002 63 (4.8) 41 (8.4)
According to the 2009 to 2018 surveillance report pub- 2001 73 (5.8) 54(11.6)
lished by the U.S. Centers for Disease Control and Preven- 2000 65 (4.6) 36 (7.9)
tion (CDC), fish was the food category most commonly 1999 61 (4.6) 30 (8.0)
implicated in foodborne outbreaks involving single food
1998 62 (4.7) 44 (11.8)
categories (CDC, 2018). From 1998 to 2018, a total of 937
Note. Data collected from the National Outbreak Reporting System (NORS).
foodborne outbreaks associated with fish were reported, a
Total fish-associated outbreaks include outbreaks with confirmed, suspected,
resulting in 5,011 illnesses, 364 hospitalization, and four and undefined etiologies. Percentage (%) of the total fish-associated out-
deaths (CDC, 2018). The number of total fish-associated breaks = (number of the total fish-associated outbreaks/number of the total
outbreaks per year declined from 62 cases in 1998 to 17 cases food-associated outbreaks) × 100%.
b
If at least one etiology was confirmed, the outbreak was considered as
in 2010. From 2011 to 2018, the number of cases increased,
a confirmed fish-associated outbreak. Percentage (%) of the confirmed
with approximately 37 outbreaks on average each year fish-associated outbreaks = (number of the confirmed fish-associated out-
(Table 1). The numbers and percentages of confirmed fish- breaks/number of the total confirmed food-associated outbreaks) × 100%.
associated outbreaks among outbreaks with at least one
confirmed etiology showed a similar trend. The percentage
of fish outbreaks in total foodborne outbreaks decreased highlight the significant challenges to fish safety and the
from 11.8% in 1998 to 2.8% in 2010. Percentages increased urgent need for better control strategies.
from 2011 to 2018, with an average of approximately 7.0% Among the 709 fish-associated outbreaks with con-
of total annual food outbreaks confirmed to be associ- firmed etiology, 99.3% were associated with one etiol-
ated with fish. Similar observations have been made by ogy (Table 2). The most common etiologies are scom-
Dewey-Mattia, Manikonda, Hall, Wise, and Crowe (2016, broid toxin or histamine (377 outbreaks), ciguatoxin (268
2018). Overall, fish and fish products have been continu- outbreaks), Salmonella spp. (15 outbreaks), and Clostrid-
ously implicated in foodborne outbreaks, contributing to ium botulinum (14 outbreaks). Scombroid poisoning is a
some 6% to 8% of total confirmed foodborne-illness out- food intoxication caused by the consumption of scombroid
breaks over recent years. This incidence is higher than the marine fish species (e.g., tuna, mahi mahi, and bluefish)
incidence of foodborne-illness outbreaks associated with that are spoiled by bacteria, which produce decarboxylase
chicken and beef, which contributed to, on average, 3.6% enzymes and convert free histidine to large quantities of
and 1.9% of total confirmed foodborne outbreaks in 2011 to histamine (Colombo et al., 2018). Ciguatoxin is produced
2017 (CDC, 2018). These fish and fish product outbreaks by Gambierdiscus toxicus and concentrated through the
T A B L E 2 The numbers and percentages of outbreaks, illnesses, and hospitalizations caused by different etiologies in confirmed
fish-associated outbreaks in the United States, 1998 to 2018
Outbreaks Illnesses Hospitalizations
Etiology No. (%) No. (%) No. (%)
Single (only one etiology involved in one outbreak)
Toxin/chemical
Scombroid toxin/histamine 377 (53.2) 1,366 (34,2) 46 (14.7)
Ciguatoxin 268 (37.8) 1,019 (25.5) 107 (34.3)
Paralytic shellfish poison 3 (0.4) 6 (0.2) 4 (1.3)
Puffer fish tetrodotoxin 1 (0.1) 5 (0.1) 2 (0.6)
Heavy metals 1 (0.1) 2 (0.1) 0 (0.0)
Others 8 (1.1) 29 (0.7) 6 (1.9)
Bacterial
Salmonella spp. 15 (2.1) 378 (9.5) 31 (9.9)
Clostridium botulinum 14 (2.0) 38 (1.0) 23 (7.4)
Shigella spp. 3 (0.4) 74 (1.9) 7 (2.2)
Staphylococcus spp. 2 (0.3) 5 (0.1) 0 (0.0)
Bacillus spp. 1 (0.1) 3 (0.1) 0 (0.0)
Campylobacter spp. 1 (0.1) 21 (0.5) 3 (1.0)
Escherichia coli O157:H7 1 (0.1) 7 (0.2) 0 (0.0)
Listeria monocytogenes 1 (0.1) 4 (0.1) 4 (1.3)
Others 1 (0.1) 5 (0.1) 0 (0.0)
Viral
Norovirus 5 (0.7) 443 (11.1) 0 (0.0)
Rotavirus 1 (0.1) 9 (0.2) 0 (0.0)
Parasitic
Anisakis 1 (0.1) 14 (0.4) 0 (0.0)
Multiple (two or more etiologies involved in one outbreak)
5 (0.7) 561 (14.1) 79 (25.3)
Total 709 3,989 312
Note. Data were collected from the National Outbreak Reporting System (NORS). Outbreaks with at least one confirmed etiology were calculated. Percentage
was calculated by dividing the number of outbreaks, illnesses, or hospitalizations caused by a specific etiology by the total number of outbreaks, illnesses, or
hospitalizations, respectively.
food chain, ultimately causing ciguatera fish poisoning in involving mahi mahi were mainly due to scombroid
humans (CDC, 2019b). Salmonella spp. contributes to a toxin/histamine. Outbreaks associated with barracuda and
large portion of all hospitalizations and was involved in Jack were mainly due to ciguatoxin. Different single eti-
the largest fish-associated outbreak of foodborne illness, ologies were identified in salmon outbreaks, 69% of which
resulting in 425 illnesses and 55 hospitalizations across 28 were due to bacteria (nine out of 13), including two out-
states in 2012, resulting from the consumption of contam- breaks of Salmonella spp., five of C. botulinum, one of E.
inated raw tuna products (Barrett, Nakao, Taylor, Eggers, coli O157:H7, and one of Bacillus cereus.
& Gould, 2017; CDC, 2012). Clostridium botulinum pro- From 1996 to 2014, imported fish were implicated in
duces a highly toxic neurotoxin and is responsible for 88 foodborne-illness outbreaks in the United States, con-
two out of four deaths (50%) in fish-associated outbreaks. tributing to 45% of outbreaks caused by imported foods
Among fish species, tuna, mahi mahi, barracuda, Jack, (Gould, Kline, Monahan, & Vierk, 2017). In the last decade,
and salmon are responsible for the most outbreaks and importation of edible fish products in the United States
illnesses in the United States (Table 3). Tuna contributed steadily increased from 5.2 billion pounds in 2009 to 6.1
to about 34% of the total confirmed fish-associated out- billion pounds in 2018, with values nearly doubled ($13.1
breaks (238 out of 709) and illnesses (1,353 out of 3,989). billion in 2009 to $22.4 billion in 2018). Although 90% to
About 97% of tuna-associated outbreaks were caused by 95% of the U.S. fish supply is imported, 35 to 38% originated
scombroid toxin/histamine and Salmonella. Outbreaks from U.S. waters (Gephart, Froehlich, & Branch, 2019;
T A B L E 3 Etiologies identified from the top five fish species that were involved in confirmed fish-associated outbreaks in the United
States, 1998 to 2018
Etiology Tunaa Mahi mahib Barracuda Jackc Salmon
Single (only one etiology involved in one outbreak)
Scombroid toxin/histamine 226 (722)d 67 (236) NA 3 (6) 3 (9)
Ciguatoxin NA 16 (60) 74 (269) 48 (227) NA
Salmonella spp. 6 (599) NA NA NA 2 (19)
Clostridium botulinum 2 (5) NA NA NA 5 (14)
Escherichia coli O157:H7 NA NA NA NA 1 (7)
Bacillus cereus NA NA NA NA 1 (3)
Staphylococcus aureus 1 (3) NA NA NA NA
Norovirus 2 (15) NA NA NA 1 (23)
Rotavirus 1 (9) NA NA NA NA
Multiple (two or more etiologies involved in one outbreak)
NA NA 1 (23)e NA NA
Total 238 (1,353) 83 (296) 75 (292) 51 (233) 13 (75)
Note. Data were collected from the National Outbreak Reporting System (NORS). The top five fish species are determined based on the sum of outbreaks and
illnesses caused by them.
a
Tuna includes food vehicles reported as tuna, ahi, albacore, yellowfin, yellowtail, and skipjack.
b
Mahi mahi includes food vehicles reported as mahi mahi and roi.
c
Jack includes food vehicles reported as Jack, amberjack, almaco jack, Hamachi, ulua, and papio.
d
Results are expressed in number of outbreaks (number of illnesses).
e
Etiologies involved in this case were ciguatoxin and Staphylococcus aureus.
Abbreviation: NA, not available.
NOAA, 2020). Besides foodborne outbreaks, pathogenic fish and fish products are well documented. A few reviews
and spoilage microorganisms have also been involved in have summarized the incidence of these pathogens in
increasing numbers of recalls of fish and fish products pro- seafoods, and the top pathogens have been reported
duced both domestically and imported from foreign coun- to be Salmonella spp., L. monocytogenes, Vibrio spp.,
tries (Table 4). The variety of recalled fish and fish products Yersinia spp., C. botulinum, S. aureus, and Aeromonas
has also increased over the years. Potential contamination spp. (Amagliani, Brandi, & Schiavano, 2012; Fernandes,
of fish products by L. monocytogenes, Salmonella, and C. Castro, Neto, & Figueiredo, 2018; Jami, Ghanbari, Zun-
botulinum led to 11 recalls from 2017 to 2019. Seven of these abovic, Domig, & Kneifel, 2014; Novoslavskij et al., 2016;
recalls were due to potential L. monocytogenes contamina- Piotrowska & Popowska, 2014; Vaiyapuri, Joseph, Rao,
tion. Salmon products were involved in all seven recalls Lalitha, & Prasad, 2019). Among them, Salmonella has
including smoked salmon and slightly salted salmon been the leading bacterial etiology for fish-associated
(FDA, 2020c). These data highlight the importance of the outbreaks. Listeria monocytogenes, despite a low incidence
control of L. monocytogenes contamination in fish and fish in fish outbreaks, is the most common bacterial cause for
products, in particular, the processed salmon products. In recalls of fish and fish products. In addition, its ubiquity
2019, elevated levels of histamine, which is caused by the in the processing environment as well as its ability to
growth of certain spoilage bacteria, were implicated in four proliferate at cold temperatures make L. monocytogenes
recalls. This highlights the need to look into the safety of a major concern for ready-to-eat (RTE) fish products.
both domestic and imported fish and fish products. Besides the aforementioned pathogens that are listed as
bacterial pathogens of greatest concern in the guidance of
Fish and Fishery Products Hazards and Controls (FDA,
2.2 Prevalence of common and 2020b), Aeromonas spp. have attracted attentions as an
emerging human pathogens in fish and fish emerging human pathogen associated with seafood prod-
products ucts (Daskalov, 2006). Aeromonas hydrophila, which is
widely distributed in aquatic environments, can not only
Based on epidemiological data from the CDC, FDA, cause diseases in both fish and human directly, but also
and U.S. Department of Agriculture (USDA) as well as increase the levels of histamine, posing a chemical hazard
survey studies reported in the scientific literature, the to human health (Bermejo, Mondaca, Roeckel, & Marti,
prevalence and the types of pathogenic microorganisms in 2003). Tables 5 and 6 summarize the latest survey studies
TA B L E 4 Fish-associated recalls in the United States, 1994 to 2019
Total numbers Total pounds
Year Fish and fish product type of recalls recalled Reasons
FDA
2019 Cold smoked salmon, smoked silver salmon, smoked 14 NA Potential Listeria monocytogenes (3),
sockeye salmon, slightly salted salmon pieces, Salmonella (1), Clostridium botulinum (2)
frozen ground tuna, yellowfin tuna, yellowfin tuna contamination, elevated level of histamine
medallions, loins, poke, steaks, ground meat and (4), and undeclared allergen (e.g., egg amd
saku, lumpfish caviar, fish ball, fish cake, and milk) (4)
smoked whitefish pate
MICROBIAL SAFETY OF FISH AND FISH PRODUCTS. . .
2018 Fish ball, fish cake, fish tofu frozen whole tilapia, 8 NA Potential Salmonella (1), Listeria
frozen Alaskan cod, frozen yellowfin tuna steaks monocytogenes (1), Hepatitis A (2)
and cubes, raw tuna, and smoked fish contamination, small pieces of plastic (1),
and undeclared allergen (e.g. egg, wheat) (3)
2017 Smoked fish, pre-sliced Nova salmon, and frozen 4 NA Potential Listeria monocytogenes
steamed Scomber fish contamination (3) and uneviscerated
products (1)
USDA
2019 Frozen sheatfish, catfish, frozen Basa fillets, frozen 13 627,286 Failure to present for import inspection (13)
yellow walking fish, frozen Mystus fish, salted egg
fish skins, frozen yellow catfish, frozen Swai fish
fillets, and frozen tilapia fillets
2018 Fresh and frozen whole catfish, catfish fillets, nuggets, 3 214,306 Leucomalachite green residue (1), failure to
and portions, smoked catfish, and Siluriformes fish present for import inspection (2)
paste and fish balls
2017 Frozen whole and catfish fillets, nuggets, steaks, raw 3 86,885 Malachite green and leucomalachite green
breaded Swai fillets, and frozen Swai fillets residue (1), misbranding and undeclared
allergen (milk) (1), failure to comply FSIS
requirements (1)
2016 Frozen Swai fillets, whole and gutted catfish, catfish 2 51,166 Crystal violet residue (1) and failure to comply
tails, fillets, steaks, trips, and nuggets FSIS requirements (1)
1994 to 2015 NA NA NA NA
Note. Data were collected from the USDA-FSIS and the FDA. Numbers in the brackets in the last column indicate the numbers of recalls associated with that particular recall reason.
Abbreviation: NA, not available.
743
744
TA B L E 5 Numbers and percentages of antibiotic-resistant Salmonella spp., Listeria monocytogenes, and Aeromonas hydrophila identified in fish and fish products in scientific literature
Numbers of
Country Fish/fish products Incidencea isolates Antimicrobial resistanceb (%) Reference
Salmonella
Brazil Retail fish 5.76 (52) 3 Trimethoprim–sulfamethoxazole (100) Cunha-Neto et al. (2019)
China Retail freshwater fish 3.5 (2,328) NA NA Li et al. (2019)
18.6 (231) 103c Tetracycline (35.9), ampicillin (28.2), Yang et al. (2015)
nalidixic acid (26.2), and
trimethoprim–sulfamethoxazole (25.2)
Retail fish NA 27 Sulfisoxazole (59.2), tetracycline (29.6), Zhang et al. (2015)
nalidixic acid (25.9), streptomycin
(22.2), and ampicillin (18.5)
India Retail fish NA 72 Ceftazidime (98.6), streptomycin (98.6), Saharan et al. (2019)
amikacin (91.7), azithromycin (79.2),
and trimethoprim (79.2)
Iran Wild fish and shrimp 6.9 (274) 19 Nalidixic acid (47.4), tetracycline (36.8), Rahimi et al. (2013)
streptomycin (15.8), and trimethoprim
(15.8)
Retail raw/fresh saltwater 2.9 (70) NA NA Zarei et al. (2012)
fish
Italy Fish products at retail stores 0.3 (2,086) NA NA Busani et al. (2005)
and in the processing
plants
Jordan Imported fish 19 (330) 64 Amoxicillin–clavulanic acid (52.2), Obaidat and Salman (2017)
cefalothin (52.2), streptomycin (49.3),
ampicillin (44.8), and kanamycin (10.4)
Malaysia Retail African catfish and 20 (30) 6 Penicillin (100), clindamycin (100), Sing et al. (2016)
African catfish collected tetracycline (100), and rifampicin (100)
from fish farm
Catfish and tilapia collected 35.9 (64) 32 Clindamycin (100), rifampicin (87.5), Budiati et al. (2013)
from retail stores and tetracycline (56.3), chloramphenicol
ponds (40.1), and spectinomycin (31.3)
Nigeria Retail catfish and catfish 11.5 (200) 23 Streptomycin (43.5), sulfamethoxazole Raufu et al. (2014)
collected from fish farms (34.8), and trimethoprim (21.7)
Saudi Imported freshwater fish 16.8 (1,678) 140 Tetracycline (90.7), ampicillin (70), and Elhadi, Aljeldah, and Aljindan
Arabia amoxicillin–clavulanic acid (45) (2016)
Spain RTE smoked salmon 1.2 (84) NA NA Cabedo, Barrot, and Canelles
(2008)
(Continues)
TA B L E 5 (Continued)
Numbers of
Thailand Retail fish and other seafood 24 (27) NA NA Ananchaipattana et al. (2014)
Retail seabass and other 21 (120) 26 Ampicillin (46), sulfisoxazole (46), Woodring et al. (2012)
seafood tetracycline (42), chloramphenicol (31),
and trimethoprim–sulfamethoxazole
(27)
Turkey Wild freshwater common 3 (100) 7 Erythromycin (100), streptomycin (57.1), Pamuk et al. (2019)
carp neomycin (42.9), and gentamicin (14.3)
Retail fish 5 (100) 5 Neomycin (80), gentamicin (20), and Onmaz et al. (2015)
trimethoprim–sulfamethoxazole (20)
Vietnam Wholesale and retail 36.6 (101) 52 Tetracycline (46.2), ampicillin (34.6), Nguyen et al. (2016)
freshwater fish chloramphenicol (30.8),

trimethoprim-sulfamethoxazole (25.0),
and nalidixic acid (11.5)
Listeria monocytogenes
Canada RTE fish products 15 (40) 6 Clindamycin (100), cefoxitin (100), Kovacevic et al. (2012)
nalidixic acid (100), amikacin (33.3),
and streptomycin (33.3)
China Retail freshwater fish 2.6 (2,328) NA NA Li et al. (2019)
Estonia RTE fish products 11.6 (7,652) NA NA Koskar et al. (2019)
European RTE fish 7.0 NA NA EFSA (2018)
Union
Greece RTE fish 6.7 (119) NA NA Soultos et al. (2014)
India Retail fish and fish products 2.2 (184) 8 Ampicillin (100), penicillin (100), Basha et al. (2019)
and fish from the landing erythromycin (100), tetracycline (100),
centers and clindamycin (100)
Retail fish 1.7 (115) NA NA Rodrigues et al. (2015)
Iran Retail rainbow trout and 9.16 (240) 22 Enrofloxacin (72.7), ciprofloxacin (68.2), Rezai et al. (2018)
rainbow trout collected tetracycline (63.6), erythromycin (40.9),
from fish farm ampicillin (31.8), and chloramphenicol
(31.8)
Fish, other seafood, and 9.5 (662) 278 Ampicillin (38.5), penicillin (38.1), Fallah et al. (2013)
environmental samples vancomycin (20.9), tetracycline (18.7),
and ciprofloxacin (17.6)
Retail fish 2.5 (80) NA NA Rahimi, Shakerian, and Raissy
(2012)
(Continues)
745
746
Numbers of
7.72 (220) NA NA Momtaz and Yadollahi (2013)
Retail saltwater fish 1.4 (70) NA NA Zarei et al. (2012)
Latvia Retail freshwater fish 26 (106)2 NANA NANA Terentjeva et al. (2015)
Wild freshwater fish (129)
Mexico Wild fish and seawater 28.1 (210) 68 Pefloxacin (28.9), cephalothin (26.7), Rodas-Suarez et al. (2006)
ampicillin (23.7), penicillin (22.5), and
ceftazidime (14.4)
Poland Fish in the processing plants 13.2 (197) 26 Penicillin (15.4), ampicillin (11.5), Skowron et al. (2019)
meropenem (11.5), erythromycin (7.7),
and cotrimoxazole (3.8)
Retail fresh and smoked fish 18.9 (301) 57 Oxacillin (57.9), ceftriaxone (31.6), and Wieczorek and Osek (2017)
clindamycin (8.8)
Spain RTE smoked salmon 8.6 (803) 69 Ampicillin (1.4) and cephalothin (1.4) Domenech,
Jimenez-Belenguer, Amoros,
Ferrus, and Escriche (2015)
Vienna Retail fish and fish products 4.9 (102) NA NA Nauman, Paulsen, Vali, and
Smulders (2014)
Aeromonas hydrophila
China Retail fish 3.8 (235) 10 Ampicillin (100), ampicillin-sulbactam Wu et al. (2019)
(100), cefazolin (100), co-trimoxazole
(90), and tetracycline (30)
Retail grass carp 31.5 (200) 63 Ampicillin (95.24), tetracycline (88.89), Yang et al. (2018)
streptomycin (79.37), nalidixic acid
(73.02), and kanamycin (53.97)
Egypt Retail frozen fish fillet 6.7 (150) 10 Streptomycin (100), cloxacillin (100), Hafez et al. (2018)
erythromycin (100), sulfamethoxazole
(80), and cefotaxime (80)
Retail tilapia and mugil 5.4 (294) 16 Cefixime (88), amoxicillin/clavulanic acid Ahmed et al. (2018)
(80), ceftazidime (80), nalidixic acid
(76), and tetracycline (72)
Fish collected from fish 47 (170) 18 Ampicillin (100), erythromycin (100), Dahdouh et al. (2016)
farms nalidixic acid (100), spectinomycin
(100), and tetracycline (66.7)
India Retail fish and fish collected 7.5 (173) 13 NA Rather et al. (2019)
from fish farms
(Continues)
Numbers of
Retail fish 33.6 (536) NA NA Vivekanandhan et al. (2005)
Iran Wild fish 19.5 (133) NA NA Rahimi, Raissy,
Razzaghimanesh, Dastgerdi,
and Shahraki (2014)
Italy Farmed and wild freshwater NA 53 Cloxacillin (100), spiramycin (100), Borella et al. (2020)
fish tilmicosin (100), ampicillin (100),
tylosin (100), and sulfadiazine (100)
Malaysia Retail fish 11.5 (87) 10 Ampicillin (100) Radu et al. (2003)
Mexico Retail frozen tilapia 0.8 (250) 2 Ampicillin (100), penicillin (100), Castro-Escarpulli et al. (2003)
carbenicillin (100), cephalothin (100),
streptomycin (100), clindamycin (199),
polymycin B (100), and rifampicin (100)
Poland Farmed carp NA 18 Ampicillin (100), penicillin (100), Guz and Kozinska (2004)
cephalothin (61), and erythromycin (56)
Turkey Retail fish 3.75 (400) NA NA Kahraman, Dumen, Issa,
Kahraman, and Ikiz (2017)
Abbreviations: NA, not available, these studies did not conduct the antibiotic resistance evaluation; RTE, ready-to-eat. .
a
Incidence: the percentage of pathogen positive samples (number of total samples tested).
b
Name of the antimicrobial (percentage of the antimicrobial-resistant isolates). Percentage of the antimicrobial resistance = (number of antimicrobial-resistant isolates/total number of isolates) × 100%. If more than five
antibiotics were tested, the results of the top five antimicrobials are shown.
747
748
T A B L E 6 Numbers and percentages of antibiotic-resistant Salmonella spp., Listeria monocytogenes, and Aeromonas hydrophila in fish and fish products in the United States based on
scientific literatures
Fish
Total Antimicrobial resistanceb
a
Pathogen Domestic Imported Incidence isolates (%) Reference
Salmonella
Salmon and tilapia 0.6 (133) 3 0 (0/3) Wang et al. (2011)
Fish NA 17 Tetracycline (5.9) and Ponce et al. (2008)
ampicillin (5.9)
Fish NA 27 Tetracycline (22.2), Zhao et al. (2006)
chloramphenicol (7.4),
nalidixic acid (7.4),
trimethoprim–
sulfamethoxazole (7.4), and
sulfamethoxazole (7.4)
Fish Fish D: 1.3 (76)c I: 12.2 NANA NANA Heinitz et al. (2000)
(2,038)
Smoked fish Smoked fish D: 0I: 3.2 (156) NA NA Heinitz and Johnson (1998)
Salmon, tilapia, and 4.1 (171) 20 Nitrofurantoin (75) Wang et al. (2011)
shrimp
Catfish fillets and 21.6 (315) 86 Cefotaxime (71) and Chen et al. (2010a); Chen,
processing clindamycin (69) Pyla, Kim, Silva, and Jung
environmental samples (2010c)
Catfish fillet 45 (80) NA NA Chen, Pyla, Kim, Silva, and
Jung (2010b)
Catfish fillet 37.5 (240) NA NA Chou, Silva, and Wang (2006)
Fish fillet 9.3 (140) NA NA Pao, Ettinger, Khalid, Reid,
and Nerrie (2008)
RTE smoked salmond 1.4 (72) NA NA Lappi et al. (2004)
(Continues)
Fish
Total Antimicrobial resistanceb
a
Pathogen Domestic Imported Incidence isolates (%) Reference

FishRTE smoked fish 3.8 (234)1.3 (233) NANA NANA Thimothe et al. (2004)
Smoked fish Smoked fish D: 13.3 (525)I: NANA NANA Heinitz and Johnson (1998)
15.2 (559)
Frozen raw salmond 36.3 (135) NA NA Eklund et al. (1995)
d
Cold-smoked salmon 78.7 (61) NA NA
Catfish fillet 36.1 (238) 80 Ampicillin (100), Bacitracin Wang and Silva (1999)
(100), chlortetracycline (5),
oxytetracycline (5), and
tetracycline (5)
Abbreviations: NA, not available, these studies did not conduct the antibiotic resistance evaluation.; RTE, ready-to-eat.
a
Incidence: percentage of pathogen positive samples (total number of samples tested);.
b
Name of the antimicrobial (percentage of the antimicrobial-resistance isolates). Percentage of the antimicrobial resistance = (number of antimicrobial-resistant isolates/total number of isolates) × 100%. If more than
five antibiotics were tested, the results of the top five antimicrobials are shown.
c
D: domestic; I: imported.
d
Samples collected from processing plants with a previously documented L. monocytogenes contamination.
749
about the incidence of Salmonella spp., L. monocytogenes, and fish products as well as their antimicrobial-resistant
and A. hydrophila in fish and fish in the world and in the properties are discussed in detail.
United States. As shown in these two tables, the highest
incidence of Salmonella spp. identified in the United
States was 1.3%. The highest incidence of Salmonella 2.2.1 Salmonella spp.
spp. identified internationally was 36.6% in Vietnam. The
highest incidences of L. monocytogenes were 78.7% and Salmonella is a genus of Gram-negative bacteria belonging
28.1% in the United States (samples were collected from to the family Enterobacteriaceae and contains the species
processing plants previously experiencing problems with S. enterica and S. bongori. Salmonella enterica is further
L. monocytogenes) and in Mexico, respectively. The inci- classified into six subspecies (enterica, salamae, arizonae,
dence of A. hydrophila in the United States was 36.1% diarizonae, houtenae, and indica) with more than 2,600
based on one study on catfish fillet, and its highest serotypes (Gal-Mor, Boyle, & Grassl, 2014). Some 99% of
incidence in the world is 47% identified in an Egyptian salmonellosis in humans is attributed to S. enterica subsp.
study. enterica, with symptoms such as diarrhea, fever, and stom-
In recent years, the occurrence of antibiotic-resistant ach cramps (Jajere, 2019). Salmonella spp. are neither nat-
bacteria (ARB) has become a significant challenge for ural inhabitants of fish nor a biological contaminant orig-
not only aquaculture but the entire food industry (Capita inally reported in fish; however, S. enterica subsp. enter-
& Alonso-Calleja, 2013; Preena et al., 2020). AMR has ica serotypes Weltevreden, Typhimurium, Javiana, Enteri-
become a global public health threat as well as an environ- tidis, Paratyphi B, Braenderup, Bovismorbificans, Thomp-
ment pollution concern (Capita & Alonso-Calleja, 2013; son, Rubislaw, Barranquilla, Heidelberg, Infantis, Group
He et al., 2020). The plasticity of bacterial communities C1, Bareilly, Nchanga, and Newport have been involved in
can enable rapid dissemination of ARGs to other microbial fish-associated outbreaks (CDC, 2018, 2019d). Salmonella
communities through horizontal gene transfer via ways can be introduced into fish and fish products through con-
such as conjugation, transformation, and transduction. tact with contaminated water, inadequate hygiene when
Mobile genetic elements (MGEs) are DNA segments that handling, and other inappropriate fish breeding, process-
can move within a genome and between different bacteria ing, or storage practices (Fernandes et al., 2018).
and include plasmids, transposons, and bacteriophages; The prevalence of Salmonella contamination in fish and
these MGEs have been shown to play a crucial role in fish products varies among different counties and is also
horizontal gene transfer and dissemination of ARGs determined by the different fish species, geographic loca-
(Alanis, 2005; Frost, Leplae, Summers, & Toussaint, tions, sampling stages (fish farm vs. retail stores), sampling
2005; Schmieder & Edwards, 2012). Plasmid-mediated parts (skin vs. intestine), sources (imported vs. domestic),
conjugation is the most common mechanism for bacteria and fish product types (raw vs. RTE). Reported contami-
to horizontally acquire resistance genes (Alanis, 2005). nation levels vary from 0.3% in Italy to 36.6% in Vietnam
Once the ARGs are transferred to a bacterium, resistance (Busani et al., 2005; Nguyen et al., 2016). In a recent survey
to antibiotics can be developed through destruction across China, 2,328 retail freshwater fish were collected,
or modification of the antibiotic itself, development and Salmonella was present at a level of 3.5% (Li et al.,
of an active efflux system to pump the antibiotic out, 2019). Carp (Cyprinus carpio) had the lowest prevalence
and/or reduction of membrane permeability to decrease of Salmonella at 1.8%, and culter alburnus (Erythrocul-
influx, modification of antibiotic receptors, alternation ter ilishaeformis) had the highest prevalence at 7.7%. In
of metabolic pathways, and other biological mechanisms this study, authors found that the northern area of China
(Alanis, 2005; Schmieder & Edwards, 2012). Food has been had the lowest incidence of Salmonella (0.5%), whereas
identified as the most important vehicle for transmitting the southern region had the highest (12.2%). Sing, Khan,
ARB and ARGs to humans, resulting in serious human Daud, and Aziz (2016) studied African catfish from four
health consequences such as treatment failure (Capita & farms and four wet markets in Malaysia; the prevalence
Alonso-Calleja, 2013). Given rising concerns over AMR, of Salmonella in the surveyed 14 retail fish (28.57%) was
the prevalence of antimicrobial-resistant Salmonella, L. higher than that in the 16 fish collected directly from the
monocytogenes, and A. hydrophila identified in fish and farms (12.5%). This highlights the fact that Salmonella is
fish products is also summarized in Tables 5 and 6. As introduced into fish and fish products during postharvest
shown in these two tables, many isolates demonstrated processing. This study also showed that fish intestines
resistance to more than one antibiotic, including critical had a higher incidence of Salmonella than skin samples.
antibiotics used for treating human and fish diseases. The prevalence was 66.67% for catfish intestine and 33.33%
In the following section, incidences of Salmonella spp., for skin. In the United States, the overall incidence of
L. monocytogenes, and A. hydrophila identified in fish Salmonella in domestic fish and fish products was lower
than the incidence in imported fish and fish products. least one antibiotic in three or more drug classes (CDC,
Salmonella was detected in 1.3% of 76 domestic raw fish 2019c). MDR has been a bigger concern as it can enhance
samples from 1990 to 1998, compared to the 12.2% preva- bacterial virulence and result in more severe diseases
lence in 2,038 samples of imported fish (Heinitz, Ruble, in patients (Brunelle, Bearson, Bearson, & Casey, 2017).
Wagner, & Tatini, 2000). Another U.S. survey study sam- Yang et al. (2015) reported that 62.5% of Salmonella
pled a total of 156 smoked fish samples from both domes- Thompson isolated from retail freshwater fish in China
tic and foreign origin; the domestic samples tested nega- demonstrated resistance to more than 14 antimicro-
tive for Salmonella, whereas five imported samples tested bials. In addition, 62.5% of Salmonella Derby and 60%
positive (Heinitz & Johnson, 1998). The prevalence of Salmonella Typhimurium showed resistance to at least six
Salmonella was lower in RTE fish products than in raw antimicrobials. All the Salmonella isolates identified from
fish, regardless of origin. For instance, Salmonella was African catfish in Malaysia were resistant to penicillin,
not detected in 89 domestic smoked fish samples, whereas clindamycin, tetracycline, and rifampicin (Sing et al.,
3.9% of 255 imported smoked fish samples tested positive 2016). About 65.6% of 72 Salmonella isolates recovered
(Heinitz et al., 2000). This underscores the importance from fish fecal samples in India showed MDR (Saharan,
of sampling, inspection, and implementation of control Verma, & Singh, 2020). In the United States, 27 Salmonella
strategies not only in domestic but also in foreign fish com- isolates were identified from imported fish: six showed
panies. resistance to antibiotics and five were resistant to at least
The predominant Salmonella serotypes isolated two antibiotics (Zhao et al., 2006). Salmonella Bareilly
from fish and fish products are as follows: Salmonella isolated from frozen dace fish and Salmonella Schwarzen-
Typhimurium and Salmonella Wandsworth (Yang grund isolated from frozen catfish were resistant to more
et al., 2015), Salmonella Potsdam (Nguyen et al., 2016), than four antibiotics. Khan et al. (2006) from the FDA
Salmonella Corvallis (Budiati et al., 2013; Sing et al., found four multidrug-resistant Salmonella strains among
2016), Salmonella Albany (Budiati et al., 2013), Salmonella 36 strains isolated from imported seafood. Salmonella Oslo
Hadar (Raufu et al., 2014), Salmonella Schwarzengrund was resistant to the most antibiotics, including ampicillin,
(Cunha-Neto et al., 2019), Salmonella Enteritidis (Rahimi, chloramphenicol, streptomycin, sulfisoxazole, tetracy-
Shakerian, & Falavarjani, 2013), and Salmonella Panama cline, and trimethoprim–sulfamethoxazole. One strain
(Pamuk, Inat, & Siriken, 2019). In the United States, the out of 17 Salmonella Weltevreden isolates from imported
most frequent Salmonella serotypes identified in imported fish showed resistance to both ampicillin and tetracy-
fish are as follows: Weltevreden, Senftenberg, Paratyphi-B, cline (Ponce et al., 2008). By contrast, three Salmonella
Lexington, Enteritidis, Newport, Thompson, Saintpaul, Typhimurium isolates recovered from imported tilapia
and Bareily (Heinitz et al., 2000; Khan et al., 2006; Ponce, did not show antimicrobial resistance (Wang et al., 2011).
Khan, Cheng, Summage-West, & Cerniglia, 2008; Zhao Though imported fish has repeatedly been identified
et al., 2006). Salmonella Tennessee was detected from with MDR bacteria, currently available studies did not
pollock fillets produced domestically; other serotypes check the AMR of Salmonella isolates from U.S. domestic
isolated from domestic seafood samples have included fish and fish products, which warrants more attention in
Salmonella Newport, Rubislaw, and Anatum (Heinitz future studies.
et al., 2000).
Antibiotic-resistant Salmonella is considered as a “Seri-
ous Threat Level pathogen” (CDC, 2019a). Unfortunately, 2.2.2 Listeria monocytogenes
Salmonella strains isolated from fish and fish products
have been shown to be resistant to a broad range of Listeria monocytogenes is a species of Gram-positive bac-
antibiotics including ampicillin, tetracycline, sulfisox- teria that has a high mortality rate of about 16% (Scallan
azole, streptomycin, trimethoprim–sulfamethoxazole, et al., 2011). The populations susceptible to L. monocyto-
nalidixic acid, ceftazidime, amikacin, azithromycin, genes infection include pregnant women, the elderly, and
trimethoprim, amoxicillin–clavulanic acid, cefalothin, immune-compromised people (Buchanan, Gorris, Hay-
kanamycin, trimethoprim, clindamycin, rifampicin, chlo- man, Jackson, & Whiting, 2017). Listeria monocytogenes
ramphenicol, spectinomycin, erythromycin, neomycin, is ubiquitous in the environment and tolerant to a broad
and gentamicin (Tables 5 and 6). The most frequently range of environmental stresses. Listeria monocytogenes
reported antimicrobials to which Salmonella has shown can grow in salt solutions with up to 14% sodium chloride
resistance are streptomycin, tetracycline, ampicillin, (Shabala, Lee, Cannesson, & Ross, 2008). It can also sur-
trimethoprim–sulfamethoxazole, nalidixic acid, trimetho- vive in freezing temperature and even grow in fish at refrig-
prim, and chloramphenicol. Some Salmonella isolates erator temperatures (Liu, Mou, & Su, 2016). Of particular
have multidrug resistance (MDR), with resistance to at concern is that L. monocytogenes can proliferate in RTE fish
products (Hunt, Blanc, Alvarez-Ordonez, & Jordan, 2018), Additional processing of fish, such as smoking and
which lack further inactivation steps before consumption. brining, can control the level of L. monocytogenes contami-
Because the prevalence of L. monocytogenes in aquatic food nation. The prevalence of L. monocytogenes decreased from
products worldwide from 1990 to 2013 has been reviewed 3.8% in raw fish to 1.3% in finished smoked fish products
by Jami et al. (2014), this discussion section focuses on the (Thimothe, Nightingale, Gall, Scott, & Wiedmann, 2004).
most recent survey studies and the prevalence of antibiotic- In a survey study conducted in Poland, L. monocytogenes
resistant L. monocytogenes isolates (Tables 5 and 6). was positive in 35.7% of fresh fish and was reduced to 5.3%
The occurrence of L. monocytogenes in fish and fish in smoked fish (Wieczorek & Osek, 2017). However, L.
products differed among countries and is also influenced monocytogenes remains a big concern in RTE fish products
by fish species, geographic locations, sampling stages, because of the pathogen’s ability to grow during cold
sampling parts, product types, and sample origins. The storage (Guyer & Jemmi, 1991) as well as the lack of ther-
incidences of L. monocytogenes in fish and fish products mal processing before consumption. The European Food
range from 1.4% (Zarei, Maktabi, & Ghorbanpour, 2012) Safety Authority (EFSA) and European Center for Disease
to 78.7% (Eklund et al., 1995). Li et al. (2019) reported Prevention and Control (ECDC) summarized the data
that the overall incidence of L. monocytogenes in freshwa- from 18 European countries, and the overall occurrence
ter fish across China was 2.6%. No L. monocytogenes was of L. monocytogenes in RTE fish products was 7.0% in
detected in Asian swamp eel (Monopterus albus), bream 2017 (EFSA, 2018). Kovacevic, McIntyre, Henderson, and
(Parabramis pekinensis), or culter alburnus (Erythroculter Kosatsky (2012) reported that 15% of RTE fish products
ilishaeformis), whereas 4.8% of loach (Misgurnus anguil- were positive for L. monocytogenes in Canada. In the
licaudatus) tested positive. The percentage of fish sam- United States, the contamination rate of the domestic RTE
ples that were positive for L. monocytogenes in the east- fish products varied from 1.3 to 1.4% (Lappi, Ho, Gall, &
ern region was 1.0% and in the central/northwestern region Wiedmann, 2004; Thimothe et al., 2004) to 78.7% (Eklund
was 3.8%. Retail fish and fish products have been reported et al., 1995). The ultrahigh contamination rate was reported
to have a higher incidence of L. monocytogenes than fish in cold-smoked salmon samples collected from six pro-
and fish products sampled at any other stage prior to processing facilities known to have encountered problems
cessing. Basha et al. (2019) collected fish and fish prod- with L. monocytogenes contamination. A 5-year survey
ucts from both retail markets and landing centers in India; study showed that 13.3 to 15.2% of domestic and imported
L. monocytogenes was detected only in retail samples, not smoked fish were positive for L. monocytogenes, unlike the
in the landing center samples. Similarly, a study in Iran incidence of Salmonella, which is lower in domestic fish
reported that 14.16% of retail rainbow trout were posi- and fish products (Heinitz & Johnson, 1998). This indicates
tive for L. monocytogenes compared to the 4.16% positive a global concern about L. monocytogenes and fish safety.
rate of fish samples collected from ponds on fish farms The presence of antibiotic-resistant isolates further
(Rezai, Ahmadi, & Salimi, 2018). Listeria monocytogenes complicates L. monocytogenes and fish safety. Listeria
was detected in 26% of retail and 2% of wild-caught fresh- monocytogenes recovered from fish and fish products
water fish in Latvia (Terentjeva et al., 2015). Fish skin is was frequently resistant to ampicillin, clindamycin, ery-
considered one primary contamination source. In a U.S. thromycin, and tetracycline. MDR was also found in 100%
study, L. monocytogenes was detected on 65.2% of skin sam- of L. monocytogenes isolated from fish and fish products in
ples from raw frozen salmon, whereas absent in flesh sam- India (Basha et al., 2019); 59.1% of strains from raw rainbow
ples from underneath the skin (Eklund et al., 1995). These trout in Iran (Rezai et al., 2018); 33% of isolates from RTE
data suggest that postharvest practices are a major point of fish in Canada (Kovacevic, Mesak, & Allen, 2012); 22.3%
L. monocytogenes contamination in fish and fish products. of isolates recovered from raw fish, other seafood, and
During the processing of fish, L. monocytogenes present environmental samples in Iran (Fallah, Saei-Dehkordi, &
on fish skin or in the environment has numerous chances Mahzounieh, 2013); 6% of strains in raw fish and seawater
to be transferred onto fillets through different handling in Mexico (Rodas-Suarez, Flores-Pedroche, Betancourt-
practices and via utensils or media such as cutting knives, Rule, Quinones-Ramirez, & Vazquez-Salinas, 2006); and
gloves of workers, and brine solutions. In a processing 3.5% of isolates identified from fresh and smoked fish in
plant known to be experiencing problems with L. monocy- Poland (Wieczorek & Osek, 2017). Although the majority
togenes, this pathogen was detected at high levels of 65% to of studies in the United States did not evaluate the AMR
67% in both raw and finished cold-smoked salmon (Eklund of L. monocytogenes isolates from fish or fish products
et al., 1995). Therefore, adequate sanitation and proper con- regardless of origin, Chen, Pyla, Kim, Silva, and Jung
trol strategies in fish processing plants are vital to reduce (2010a) reported that 71% and 69% of L. monocytogenes
the risk of L. monocytogenes contamination in fish and fish isolates recovered from domestic catfish fillets and the
products. processing environment were resistant to cefotaxime
and clindamycin, respectively. Among L. monocytogenes to Salmonella and L. monocytogenes, A. hydrophila has a
isolated from imported fish and other seafood, 75% were higher incidence in retail fish than in fish collected from
resistant to nitrofurantoin (Wang et al., 2011). fish farms. An Indian study reported that the prevalence
of A. hydrophila in swab samples from gills of fish from
retail markets and farms was 44% and 28%, respectively
2.2.3 Aeromonas hydrophila (Rather, Willayat, Wani, Hussain, & Shah, 2019). These sur-
face bacteria can cross-contaminate the fish flesh and the
Aeromonas spp. is a common cause of fish disease, with contact surfaces of equipment during processing. It has
the two most frequent strains causing disease being A. been reported that fish fillets have a higher incidence of A.
hydrophila and A. salmonicida (Hayatgheib, Moreau, hydrophila (33.3%) than whole fish (10% to 12.5%) (Hafez,
Calvez, Lepelletier, & Pouliquen, 2020). Aeromonas Darwish, Elbayomi, Hussein, & El Nahal, 2018). Similarly,
hydrophila is not only a fish pathogen but also a zoonotic when 238 domestic processed catfish fillets were examined
pathogen that can cause human diseases such as gas- for the presence of A. hydrophila in the United States, the
troenteritis, septicemia, and traumatic and aquatic wound pathogen was isolated from 36.1% of the samples (Wang &
infections (Daskalov, 2006; Stratev & Odeyemi, 2016). Silva, 1999). This evidence again emphasizes the vital role
The wide distribution of A. hydrophila in the aquatic of processing facilities in ensuring fish product safety.
environment as well as its ability to survive or even grow Resistance to antibiotics in A. hydrophila isolates from
in foods at cold temperatures further make the pathogen fish and fish products has been frequently reported inter-
a big concern in food safety (Daskalov, 2006). Aeromonas nationally (Tables 5 and 6). Aeromonas hydrophila strains
hydrophila is frequently isolated from fish and fish prod- are commonly resistant to ampicillin, tetracycline, and
ucts. The incidence varies from 0.8% in retail frozen tilapia streptomycin. A 100% resistance rate to ampicillin in all A.
collected from Mexico City (Castro-Escarpulli et al., 2003) hydrophila isolates has been reported repeatedly (Borella
to 47% in farmed fish from Egypt (Dahdouh, Basha, Khalil, et al., 2020; Castro-Escarpulli et al., 2003; Dahdouh et al.,
& Tanekhy, 2016). A high incidence of over 30% was also 2016; Guz & Kozinska, 2004; Radu et al., 2003; Wang
reported in catfish fillets collected from processing plants & Silva, 1999; Wu et al., 2019). In addition, multidrug-
in the United States (Wang & Silva, 1999), retail grass carp resistant strains were also detected at high rates in A.
in China (Yang et al., 2018), and retail fish from India hydrophila isolates from fish and fish products. In partic-
(Vivekanandhan, Hatha, & Lakshmanaperumalsamy, ular, all A. hydrophila isolates recovered from retail fish
2005). in Malaysia (Radu et al., 2003), retail frozen fish fillets or
The occurrence of A. hydrophila in fish varies by sea- farmed fish in Egypt (Dahdouh et al., 2016; Hafez et al.,
son, fish species, sampling parts, sampling stages, and 2018), and farmed and wild freshwater fish in Italy (Borella
product types. Wang and Silva (1999) reported that the et al., 2020) were resistant to at least three antibiotics.
highest incidence of A. hydrophila in catfish fillets from Multidrug-resistant A. hydrophila against ampicillin, bac-
the United States was in summer. Vivekanandhan et al. itracin, and tetracycline (tetracycline, oxytetracycline, or
(2005) did not find a correlation with sampling time and chlortetracycline) has also been detected in U.S. domes-
A. hydrophila prevalence in a 3-year survey study of retail tic catfish fillets (Wang & Silva, 1999). In the United
fish in India, however. The different results from these States, drugs can be given to sick fish via immersion,
two studies might result from the different geographic injection, or medicated feed. Among these three methods,
locations and different weather conditions in these two medicated feed has been commonly used and has been
countries. In a Malaysian survey study, A. hydrophila was accepted as a more effective and safer method than the
found in 10 to 16% of tilapia (Tilapia mossambica), keli other two methods (Bai, Katya, & Yun, 2015). Four drugs
(Clarias batrachus), and puyu (Anabas testudineus) but have been approved for making medicated feed, including
not in terubuk (Tenualosa toli) (Radu, Ahmad, Ling, & oxytetracycline dihydrate, sulfadimethoxine/ormetoprim,
Reezal, 2003). The occurrence of A. hydrophila in differ- sulfamerazine (fish grade), and florfenicol (FDA, 2020a).
ent parts of fish is also fish-species dependent. For exam- The identification of multidrug-resistant pathogens from
ple, A. hydrophila was isolated from nine viscera samples fish and fish products, especially pathogens resistant to
(6.3%) but no muscle samples among 144 mugil samples both human and aquaculture drugs, highlights the criti-
collected from retail stores in Egypt (Ahmed, Mohamed, cal importance of prudent antibiotic usage in aquaculture
Rezk, Gharieb, & Abdel-Maksoud, 2018). For tilapia, on and the urgent need for research and strategies to mitigate
the other hand, A. hydrophila was detected in 2.7% of AMR.
muscle and 2.0% of intestine samples. Different process- To sum up, human pathogens including Salmonella, L.
ing and handling methods are also factors that deter- monocytogenes, and A. hydrophila have been detected at
mine A. hydrophila prevalence in final products. Similar varying rates in fish and fish products across the world. In
the era of globalization, it is extremely important yet diffi- inoculated in gilthead seabream fillets at 6.5 to 7 log CFU/g
cult to ensure the safety of fish and other aquaculture prod- increased to ∼9 log CFU/g after 16 days of storage at 4 ◦ C,
ucts, considering the diverse regulations in different coun- whereas the population was maintained at 0 ◦ C (Provin-
tries. The issue is further complicated by the diversity of cial et al., 2013). The impact of temperature can be fur-
fish species, geographic locations, sampling stages, sam- ther modulated by the application of different packaging.
pling parts, and product types. In general, retail fish and For example, when smoked blue cod was stored at 3 ◦ C
fish products have a higher incidence of human pathogens in vacuum packs, the A. hydrophila population increased
than fish collected from fish farms, highlighting the vital from ∼5 to 8.5 log CFU/g in 10 days, whereas the com-
role of processing plants in fish safety. Fish products can be bination of –1.5 ◦ C and carbon dioxide packs gradually
contaminated not only by the human pathogens originally reduced bacterial population to ∼3 log CFU/g after 155
existing in a processing plant, but by pathogens transferred days (Bell, Penney, & Moorhead, 1995). Listeria monocyto-
from contaminated raw materials to finished fish prod- genes in seabream fillets packaged in 60 to 80% CO2 and
ucts, processing equipment, and personnel. This results in 40 to 20% N2 was reduced by 1.5 log CFU/g after 16 days
a cascade of cross-contamination and re-contamination. of storage at 0 ◦ C, compared with an over 2 log CFU/g
Once the pathogens are introduced into fish products, increase in air-packaged fillets stored at 4 ◦ C (Provincial
they are very challenging to eliminate and can pose et al., 2013). The L. monocytogenes population in vacuum-
huge safety concerns during subsequent distribution and packaged rainbow trout fillets decreased from 4.48 to 3.13
storage. log CFU/g during storage at 4 ◦ C for 20 days (Dimitrijevic
et al., 2019).
Given that the occurrence of L. monocytogenes in RTE
2.3 Survival of common and emerging fish products has been well documented, many studies
human pathogens in fish products have evaluated the survival of L. monocytogenes in smoked
fish products, particularly smoked salmon. Rørvik (2000)
Because of concerns about human pathogens identified in reviewed the storage studies of L. monocytogenes in hot-
fish and fish products, numerous studies have evaluated and cold-smoked salmon in the 1990s. Nowadays, L. mono-
the survival of human pathogens in fish products (Table 7). cytogenes is a continuing challenge in RTE fish products.
As indicated in Table 7, the populations of Salmonella inoc- Even in naturally contaminated cold-smoked salmon with
ulated on fish products generally maintained at similar lev- less than 0.2 CFU/g of L. monocytogenes, the bacterial
els or declined during cold storage. Populations of L. mono- population increased to 2,700 CFU/g after 8 to 15 days of
cytogenes and A. hydrophila generally increased during storage at 4 ◦ C to mimic a controlled cold chain, followed
refrigeration storage. The behavior of human pathogens by a 7-day storage at 8 ◦ C to simulate a domestic setting
in fish products is further influenced by bacteria species, (Beaufort et al., 2007). In challenge studies, the survival
inoculation levels, storage temperatures, and packaging of L. monocytogenes is dependent on storage temperatures
methods. For instance, when ∼3 log CFU/g of Salmonella and packaging methods. During frozen storage at –20 ◦ C,
Weltevreden was inoculated in yellowfin tuna, the bacte- L. monocytogenes in smoked salmon decreased slightly
rial population decreased by ∼0.5 log CFU/g after 84 days from 2.5 to 2.1 log MPN/g (McCarthy, 1997). During
of storage at −18 ◦ C, whereas Salmonella Newport inoc- refrigeration storage, a higher temperature promotes L.
ulated at the same level reduced by more than 2.0 log monocytogenes growth. In a recent study, the population of
CFU/g after storage (Liu et al., 2016). In the same study, L. L. monocytogenes in sliced, vacuum-packed cold-smoked
monocytogenes SFL0404 at an initial level of ∼3 log CFU/g salmon increased from ∼2 to 5–5.5 log CFU/cm2 after 29
decreased by ∼1.5 log CFU/g at the end of frozen storage, days of storage at 4 ◦ C (Heir, Liland, Carlehog, & Holck,
whereas the population was maintained when the inocu- 2019). When the storage temperature increased to 8 ◦ C,
lation level was ∼6 log CFU/g. The survival/growth rate of L. monocytogenes grew to 7 to 8 log CFU/cm2 . During
pathogens increases with the increase of storage tempera- cold storage for 42 days at 2 ◦ C, L. monocytogenes in
ture. At a room temperature of 26 ◦ C, the Salmonella pop- hot-smoked rainbow trout fillets packaged in 100% CO2
ulation in red grouper increased from ∼4 to ∼7 log CFU/g maintained at ∼4.3 log CFU/g, compared to a rapid growth
after 7 days (Kumar, Datta, & Lalitha, 2015). When stored in vacuum-packed hot-smoked rainbow trout fillet, where
at 4 and –20 ◦ C, however, bacterial populations decreased bacterial population increased to 7.9 log CFU/g (Tosun &
to ∼2 log CFU/g and less than 1 log CFU/g after 7 days, Ozden, 2014). The above evidence, collectively, proves the
respectively. Rajkowski and Sommers (2012) even observed ability of selected human pathogens to survive or grow
a 1.6 log CFU/g increase of Salmonella spp. in catfish fil- in fish products during distribution or storage at both
lets after 10 days of storage at 4 ◦ C. Listeria monocytogenes commercial and consumer levels.
TA B L E 7 Survival of Salmonella spp., Listeria monocytogenes, and Aeromonas hydrophila in fish products under different storage conditions
Bacterial
Storage Inoculation population
Pathogen Fish species Sample typea Storage condition time level post-storage Unit Reference
Salmonella
Carp, common Fish patty, 4 ◦ C, foam plates 5 days 7.12 6.80 Log CFU/g Ilhak and Guran
(Cyprinus carpio) cooked wrapped with plastic (2014)
wrap
Fillet 0 ◦ C, wooden box 15 days 6.2 6.2 Log CFU/g Tassou,
covered with ice and Lambropoulou, and
stored aerobically Nychas (2004)
Catfish (Ictalurus Fillet 4 ◦ C, plastic bag 10 days 2.4 4.0 Log CFU/g Rajkowski and
punctatus) Sommers (2012)
−20 ◦ C, plastic bag 12 months 4.4 3.7 Log CFU/g

◦
Mackerel (Rastrelliger Fillet −20 C 7 days ∼4 <1 Log CFU/g Kumar et al. (2015)
kanagurta)
4 ◦C 7 days ∼4 ∼2 Log CFU/g
◦
26 C (room 7 days ∼4 ∼7 Log CFU/g
temperature)
Red grouper Cube 4 ◦ C, Whirl-Pak bag 4 days 6.13 3.69 Log CFU/g Kim, Marshall,
(Epinephelus morio) Cornell, Iii, and
Wei (1995)
Salmon (Salmo salar) Fillet 2 ◦ C, plastic bag 3 days 5.38 4.39 Log CFU/g Tosun, Alakavuk,
Ulusoy, and Erkan
(2018)
Seabream (Sparus Fillet 4 ◦ C, individually 16 days 6.4 to 6.8 ∼6.5 Log CFU/g Provincial et al. (2013)
aurata) packaged in trays, air
0 ◦ C, individually 16 days 6.4 to 6.8 4.5 to 5 Log CFU/g
packaged in trays, air
4 ◦ C, individually 16 days 6.4 to 6.8 4 to 5 Log CFU/g
packaged in trays,
MAP
0 ◦ C, individually 16 days 6.4 to 6.8 4 to 5 Log CFU/g
packaged in trays,
MAP
Yellowfin tuna Cube 5 to 7 ◦ C, sealed 14 days 2.5 to 3 ∼1.5 Log CFU/g Liu et al. (2016)
stomacher bag
14 days 4 to 5 3 to 4 Log CFU/g
(Continues)
755
756
Bacterial
−18 ◦ C, sealed 84 days ∼3 <1 to 2.5 Log CFU/g
stomacher bag
84 days 4.5 ∼2.5 Log CFU/g
Hake Fillet 4 ◦ C, sealed Ziploc bag 7 days ∼3.0 4.8 Log CFU/cm2 Banos et al. (2016)
◦
Carp, silver Minced 4 C, packaged tightly 12 days 4.6 4.92 Log CFU/g Abdollahzadeh,
(Hypophthalmichthys in plastic bag Rezaei, and
molitrix) Hosseini (2014)
Carp, common Fish patty, 4 ◦ C, foam plates 5 days 7.16 7.80 Log CFU/g Ilhak and Guran
cooked wrapped with plastic (2014)
wrap
Carp, common Fillet 0 ◦ C, wooden box 15 days 4.8 6.5 Log CFU/g Tassou et al. (2004)
(Cyprinus carpio) covered with ice and
stored aerobically
Carp, grass Slice 4 ◦ C, vacuum packaged 16 days 4.61 ∼8.2 Log CFU/g Langroudi et al. (2011)
(Ctenopharyngodon
idella)
Catfish (Ictalurus Fillet 4 ◦ C, plastic bag 10 days 3.0 5.8 Log CFU/g Rajkowski and
punctatus) Sommers (2012)
−20 ◦ C, plastic bag 12 months 5.3 5.0 Log CFU/g
◦
Fillet 4 C, individually 14 days 4.6 ∼8.2 Log CFU/g Kin et al. (2012)
packed in Ziploc bag
Catfish, African (Clarias Minced 4 ◦ C, tightly packaged 14 days 4.3 6.82 Log CFU/g Alsaggaf, Moussa,
gariepinus) in plastic bags Elguindy, and Tayel
(2017)
Dolphinfish Fillet 20 ◦ C, vacuum 4 days ∼3.5 ∼7.2 Log CFU/g Montero,
(Coryphaena packaged in flexible Gomez-Estaca, and
hippurus) bags Gomez-Guillen
(2007)
Kachlan (Ttrachinotus Fillet 10 ◦ C 12 days 4.6 5.95 Log CFU/g Al-Hajj et al. (2017)
ovatus Linnaeus)
Mahi mahi (Coryphaena Fillet 4 ◦C 10 days 2.55 7.91 Log CFU/g McCarthy and
hippurus) Burkhardt (2012)
Red mullet (Mullus Fillet 0 ◦ C, wooden box 15 days 5.8 6.3 Log CFU/g Tassou et al. (2004)
barbatus) covered with ice and
stored aerobically
(Continues)
Bacterial
◦
Trout, rainbow Minced 4 C, zipper packs, 12 days ∼5 8.3 Log CFU/g Mirahmadi,
(Oncorhynchus aerobic Aminzare, Azar,
mykiss) and Kamali (2020)
Fillet 4 ◦C 16 days 6.23 8.8 Log CFU/g Sharifi, Khanzadi,
Hashemi, and
Azizzadeh (2017)
Slice 4 ◦ C, sealed 15 days ∼3 7.38 Log CFU/g Alboofetileh, Rezaei,
nylon/polyethylene Hosseini, and
pouches Abdollahi (2016)
Fillet 4 ◦ C, vacuum packaged 20 days 4.48 3.13 Log CFU/g Dimitrijevic et al.
(2019)
Fillet, 2 ◦ C, vacuum packaged 42 days 4.32 7.90 Log CFU/g Tosun and Ozden
hot-smoked in plastic film bag (2014)
2 ◦ C, MAP in plastic 42 days 4.32 4.25 Log CFU/g
film bag
Piece, 7 ◦ C, sealed plastic film 30 days ∼2.0 ∼7.0 Log CFU/g Shin, Kang, and Rasco
hot-smoked with low oxygen (2008)
permeability
Seabass (Dicentrarchus Fillet 4 ◦ C, vacuumed 21 days 3.26 6.58 Log CFU/g Boulares, Mankai,
labrax) packaged into Sadok, and
polyethylene boxes Hassouna (2017)
Fillet 4 ◦ C, modified MAP 15 days ∼4 ∼8 Log CFU/g Bolívar et al. (2018)
Fillet 9 ◦ C, modified MAP 6 days ∼4 ∼7.5 Log CFU/g
Seabream, gilthead Fillet 4 ◦ C, modified MAP 15 days ∼4 ∼8 Log CFU/g Bolívar et al. (2018)
(Sparus aurata)
Fillet 4 ◦ C, modified MAP 6 days ∼4 ∼7 Log CFU/g
◦
Fillet 4 C, individually 16 days 6.5 to 7 ∼9 Log CFU/g Provincial et al. (2013)
0 ◦ C, individually 16 days 6.5 to 7 6.5 to 7 Log CFU/g
4 ◦ C, individually 16 days 6.5 to 7 8 to 9 Log CFU/g
packaged in trays,
MAP
(Continues)
757
758
Bacterial
◦
0 C, individually 16 days 6.5 to 7 5 to 5.5 Log CFU/g
packaged in trays,
MAP
Salmon (Salmo salar) Fillet 2 ◦ C, plastic bag 3 days 4.8 4.95 Log CFU/g Tosun et al. (2018)
◦
Piece 7 C 8 days 4.8 7.6 Log CFU/g Montiel, Bravo, and
Medina (2013)
Fillet 4 ◦ C, sealed Ziploc bag 7 days ∼2.5 4.3 Log CFU/cm2 Banos et al. (2016)
Fillet 4 ◦ C, sealed Ziploc bag 10 days 1.6 2.6 Log CFU/g Soni and
Nannapaneni
(2010)
Slice, 4 ◦ C, vacuum packaged 29 days ∼2 5 to 5.5 Log CFU/cm2 Heir et al. (2019)
cold-smoked
8 ◦ C, vacuum packaged 29 days ∼2 7 to 8 Log CFU/cm2
Fillet, smoked 4 ◦ C, sealed Ziploc bag 7 days ∼3 6.15 Log CFU/cm2 Banos et al. (2016)
◦
Piece, smoked 4 C, vacuum packaged 28 days ∼4 ∼6.3 Log CFU/cm2 Concha-Meyer,
Schöbitz, Brito, and
Fuentes (2011)
Slice, 4 ◦ C, individually 15 days ∼3.5 4.5 Log CFU/g Tahiri, Desbiens,
cold-smoked packed in Kheadr, Lacroix,
oxygen-permeable and Fliss (2009)
film
Smoked −20 ◦ C 7 days 2.5 2.1 Log MPN/g McCarthy (1997)
◦
Yellowfin tuna Cube 5 to 7 C, sealed 14 days ∼2.5 ∼6 Log CFU/g Liu et al. (2016)
stomacher bag
14 days 4 to 5 ∼8 Log CFU/g
◦
−18 C, sealed 84 days 3 to 3.5 2 to 3.5 Log CFU/g
stomacher bag
84 days ∼6 ∼6 Log CFU/g
(Continues)
Bacterial
Carp, grass Fillet 4 ◦ C, packaged in sterile 16 days 3.74 ∼9 Log CFU/g Wang et al. (2017))
(Ctenopharyngodon polyvinyl chloride
idellus) bag
Catfish (Ictalurus Fillet 4 ◦C 15 days 4.5 7.0 Log Fernandes, Flick, and
punctatus) CFU/100 g Thomas (1998)
Cod, blue (Parapercis Piece, smoked 3 ◦ C, vacuum packaged 21 d ∼5 ∼8.5 Log CFU/g Bell et al. (1995)
colias)
−1.5 ◦ C, vacuum 42 d ∼5 ∼8 Log CFU/g
packaged
3 ◦ C, carbon dioxide 42 d ∼5 ∼6.5 Log CFU/g
packaged
−1.5 ◦ C, carbon dioxide 155 d ∼5 ∼3 Log CFU/g
packaged
Trout, rainbow Fillet 4 ◦C 15 days 4.5 7.2 Log Fernandes et al. (1998)
(Oncorhynchus CFU/100 g
mykiss)
Seabream, gilthead Skin and gill 1 to 8 ◦ C (fluctuating) 21 days ∼4 ∼9 Log CFU/g Giuffrida, Ziino,
(Sparus aurata) Valenti, Donato,
and Panebianco
(2007)
a
Samples without any additional note were raw samples.
Abbreviation: MAP, modified atmosphere packaged.
759
2.4 Spoilage microorganisms and the packaged red drum and MAP-packaged (50% CO2 and
formation of chemical hazards 50% N2 ) hake fillet microbiota consisted of Brochothrix
and Photobacterium, respectively (Antunes-Rohling et al.,
In addition to concerns about the contamination and 2019; Silbande et al., 2018). The dominant microbiota as
proliferation of human pathogens in fish and fish prod- well as other fish microbiota have demonstrated varying
ucts, the growth of certain spoilage bacteria can cause degrees of histamine production after storage. For exam-
a chemical safety concern. These spoilage bacteria result ple, Wang et al. (2017) reported that after 16 days of stor-
in increased levels of histamine, which causes scombroid age at 4 ◦ C, histamine production in Pseudomonas jessenii-
toxin/histamine poisoning. A wide range of bacteria are inoculated grass carp increased from 1.9 to 23.7 mg/kg,
capable of producing histamine, including Morganella compared to 1.6 mg/kg in the noninoculated control. In in
morganii, Klebsiella pneumoniae, Hafnia alvei, Morganella vitro testing, one isolate of Aeromonas salmonicida exhib-
psychrotolerans, Acinetobacter lwoffii, Plesiomonas shigel- ited strong histamine-producing ability with the maxi-
loides, Pseudomonas spp., Photobacterium spp., Aeromonas mum production rate of 115 mg/L (Hu, Huang, & Chen,
spp., Vibrio spp., Clostridium spp., Proteus spp., Serratia 2014). Therefore, effective quality control strategies against
spp., Enterobacter spp., and Staphylococcus spp. (Biji, Rav- fish spoilage microbiota are important for fish chemical
ishankar, Venkateswarlu, Mohan, & Gopal, 2016). Consid- safety.
ering the important role of the fish spoilage microbiome As indicated in Table 8, microbial identification in
in fish chemical safety, greater efforts have been put into recent studies is mainly carried out using culture-
understanding the microbial population changes during independent sequencing or analysis methods. Compared
fish and fish product storage. Thanks to the development with culture-dependent methods, which involve culture
and application of NGS, in-depth information is being isolation and identification using selective agar and a series
obtained about the dynamic microbial population changes of biochemical tests (Montes, Perez, & Nieto, 1999; Shewan,
during processing and storage. These recent advances in Hobbs, & Hodgkiss, 1960), culture-independent methods
fish microbiome analysis and their dynamics during stor- require less time and labor. The gene of choice has been
age are summarized in Table 8. 16S rRNA because of its mosaic structure and the availabil-
The initial fish microbiota is commonly dominated by ity of a growing database (Ringø et al., 2016). Duan, Zhou,
Acinetobacter, Pseudomonas, Photobacterium, Arthrobac- Xiao, Miao, and Zhao (2019) utilized polymerase chain
ter, Aeromonas, Psychrobacter, Shewanella, and Chry- reaction (PCR) amplification of 16S rRNA coupled with
seobacterium. Despite the wide range of bacterial genera, denaturing gradient gel electrophoresis (DGGE) and iden-
only a small portion of the microbiota, namely, specific tified the major spoilers of tilapia fillets during cold aerobic
spoilage organisms, can outcompete the other bacteria, storage as Pseudomonas sp., Shewanella putrefaciens, and
grow to high numbers under certain storage conditions, Psychrobacter sp. High-throughput sequencing has been
and produce metabolites that ultimately lead to sensory suggested to have a better quantification reliability than
rejection of the product (Boziaris & Parlapani, 2017). Dur- PCR–DGGE in identification of fish spoilage microbiota.
ing cold storage, the genera Pseudomonas, Shewanella, For example, 16S rRNA DGGE detected Aeromonas sp. and
Aeromonas, Photobacterium, Brochothrix, and Serratia Pseudomonas spp. in crisp grass carp fillets stored at 4 ◦ C in
gradually dominate the fish microbiota. In general, the air after 10 days, whereas 16S rRNA amplicon sequencing
spoilage microbiota in fish stored in air are Pseudomonas, quantitatively identified Aeromonas (38.8%), Pseudomonas
Shewanella, and Aeromonas, whereas Brochothrix, Serra- (37.4%), Acinetobacter (13.4%), unclassified Enterobacte-
tia, and Photobacterium are the major microbiota of fish riaceae (∼3%), unclassified Pseudomonadaceae (∼3%), as
stored in reduced oxygen conditions such as vacuum pack- well as other bacterial genera (Pan, Li, Shen, Chen, &
aging and modified atmosphere packaging (MAP). It is Li, 2018). In recent years, the internal spacer region
reported that after cold storage in air, Pseudomonas con- between 16S and 23S rRNA and single-copy target genes
tributed to over 60% of the microbiota of fillets of grass (e.g., rpoB and recA) have also been used to facilitate
carp (Sun, Hong, Jia, Liu, & Luo, 2020), blunt snout the identification of key spoilage microorganisms and
bream (Li et al., 2018), seabream (Parlapani, Kormas, & to gain a comprehensive overview of the active bacte-
Boziaris, 2015), bighead carp (Zhuang et al., 2019), com- rial populations in fish (Mayo et al., 2014; Syrova et
mon carp (Zhang, Li, Li, Liu, & Luo, 2015), silver carp al., 2018).
(Jia et al., 2018), cod (Sørensen, Bøknæs, Mejlholm, & Dal- In addition to determining the spoilage taxonomic
gaard, 2020), plaice (Zotta, Parente, Ianniello, De Filip- composition, shotgun metagenomic sequencing has led
pis, & Ricciardi, 2019), Atlantic salmon (Wang et al., 2019), to the discovery of ARGs in those microbial commu-
and Russian sturgeon (Chen et al., 2020). Under reduced nities (Schmieder & Edwards, 2012; Yukgehnaish et al.,
oxygen cold storage at 4 ◦ C, about 50% of the vacuum- 2020). Shotgun metagenomics is defined as “untargeted
TA B L E 8 Microbial changes of fish and fish products during cold storage
Key taxa before treatment Key taxa after treatment
Detection Processing or or storage and their relative or storage and their
Fish method storage condition abundance (%)a relative abundance (%)a Reference
◦
Blunt snout bream 16S rRNA 4 C, 8 days, air Acinetobacter (22), Pseudomonas (65), Li et al. (2018)
(Megalobrama amplicon Pseudomonas (22), and Shewanella (20), and
amblycephala) sequencing on Kocuria (10) Aeromonas (8)
Illumina MiSeq
Seabream (Sparus aurata) 16S rRNA Sanger 0 ◦ C, 14 days, air Pseudomonas (55), Pseudomonas (80) and Parlapani et al. (2015)
sequencing Psychrobacter (32), and Shewanella (20)
Macrococcus (13)
16S rRNA Sanger 0 ◦ C, 20 days, air Acinetobacter (34), Shewanella Pseudomonas (75) and Parlapani, Meziti,
sequencing (29), and Pseudomonas (26) Shewanella (25) Kormas, and
Boziaris (2013)
Bighead carp (Aristichthys 16S rRNA 4 ◦ C, 8 days, air Photobacterium (49.6), Pseudomonas (∼60), Zhuang et al. (2019)
nobilis) amplicon Acinetobacter (10.1), and Aeromonas (∼18), and
sequencing on Aeromonas (∼4.2) Shewanella (∼6)
Illumina MiSeq
16S rRNA Sanger 4 ◦ C, 8 days, air Acinetobacter (37), Aeromonas Aeromonas (82) and Liu, Zhang, Li, and
sequencing (27), and Kocuria (17) Pseudomonas (18) Luo (2017)
Grass carp (Ctenopharyngodon 16S rRNA 4 ◦ C, 6 days, air Acinetobacter (30.76), Kocuria Pseudomonas (83.10), Sun et al. (2020)
idellus) amplicon (11.57), and Pseudomonas Acinetobacter (5.89), and
sequencing on (10.06) Shewanella (5.46)
Illumina MiSeq
16S rRNA Lightly salted, 4 Pseudomonas (25) and Pseudomonas (> 20) and Zhang et al. (2019)
◦
amplicon C, 8 days, air, Acinetobacter (20) Psychrobacter (> 20)
sequencing on
Illumina MiSeq
16S rRNA 4 ◦ C, 10 days, air Acinetobacter (53.3), Aeromonas (38.8), Pan et al. (2018)
amplicon Wautersiella (6.3), and Pseudomonas (37.4), and
sequencing on unclassified Alcaligenaceae Acinetobacter (13.4)
Illumina HiSeq (4.4)
Common carp (Cyprinus 16S rRNA Sanger 4 ◦ C, 8 days, air Acinetobacter (52.8) and Pseudomonas (100) Zhang et al. (2015)
carpio) sequencing Moraxella (13.2)
(Continues)
761
762
Key taxa before treatment Key taxa after treatment
Detection Processing or or storage and their relative or storage and their
Fish method storage condition abundance (%)a relative abundance (%)a Reference
◦
Silver carp 16S rRNA 4 C, 6 days, air Pseudomonas (22.0), Pseudomonas (79.8), Jia et al. (2018)
(Hypophthalmichthys amplicon Aeromonas (20.5), and Aeromonas (6.5), and
molitrix) sequencing on Acinetobacter (8.1) Acinetobacter (4.7)
Illumina MiSeq
Cod (Gadus morhua) 16S rRNA -2 ◦ C, 32 days, air Acinetobacter (38.3), Pseudomonas (86.4), Sørensen et al. (2020)
amplicon Pseudomonas (34.1), and Psychrobacter (5.9), and
sequencing on Photobacterium (5.5) Shewanella (3.4)
Illuminia MiSeq
16S rRNA 4 ◦ C, 3 days, air Pseudomonas (∼5), Photobacterium (∼86), Kuuliala et al. (2018)
amplicon Acinetobacter (∼3), and Acinetobacter (∼6), and
sequencing on Flavobacterium (∼3) Pseudomonas (∼4)
Illumina MiSeq
Red drum (Sciaenops ocellatus) 16S rRNA 4 ◦ C, 8 days, Arthrobacter (11.9), Brochothrix (50.0), Silbande et al. (2018)
amplicon Vacuum Chryseobacterium (10.3), Carnobacterium (19.6),
sequencing on packaged and Brevibacterium (8.5) and Pseudomonas (8.7)
Illumina MiSeq
Hake (Merluccius merluccius) 16S rRNA 4 ◦ C, 5 days, MAP Psychrobacter (93.9), Photobacterium (46), Antunes-Rohling
amplicon (50% CO2 , 50% Carnobacterium (3.2), and Moritella (25), and et al. (2019)
sequencing on N2 ) Photobacterium (1.8) Psychrobacter (20)
Illumina MiSeq
Atlantic horse mackerel 16S rRNA Sanger 6 ◦ C, 5 days, MAP Photobacterium (16.1), Serratia (28.6), Alfaro and
(Trachurus trachurus) sequencing (48% CO2 , 50% Arthrobacter (12.9), and Carnobacterium (22.1), Hernandez (2013)
N2 , 2% O2 ) Carnobacterium (11.0) and Shewanella (16.9)
Tilapia (Oreochromis niloticus) 16S rRNA 4 ◦ C, 12 days, air Pseudomonas, Acinetobacter, Pseudomonas, Shewanella, Duan et al. (2019)
PCR-DGGE and Brevibacterium and Psychrobacter
Atlantic salmon 16S rRNA 4 ◦ C, 3 days, air Shewanella (27.9), Pseudomonas (68.7), Wang et al. (2019)
amplicon Photobacterium (13.7), and Shewanella (11.9), and
sequencing on Pseudomonas (12.3) Acinetobacter (9.7)
Illumina MiSeq
Russian sturgeon (Acipenser 16S rRNA 4 ◦ C, 12 days, air Chryseobacterium (34.3), Pseudomonas (> 95) Chen et al. (2020)
gueldenstaedtii) amplicon Acinetobacter (18.2), and
sequencing on Serratia (15.6)
Illumina MiSeq
a
If multiple genera are mentioned in the literature, only the top three were listed.
Abbreviation: MAP, modified atmosphere packaged.
F I G U R E 1 Sources that can contribute or transfer pathogens, antibiotic-resistant bacteria, and antibiotic-resistant genes to the final fish
and fish products
sequencing (shotgun) of all (meta) microbial genomes 3 CONTAMINATION SOURCES

(genomics) present in a sample” (Quince, Walker, Simp-
son, Loman, & Segata, 2017). This technique is a power- The environment is considered the most important deter-
ful tool for comprehensively profiling the gene functions minant of the microbiota of fish and fish products
of the microbiota. In terms of ARGs, shotgun metage- (Yukgehnaish et al., 2020). As shown in Figure 1, a variety
nomics includes extraction of DNA from samples, cre- of sources and factors can also contribute to the pathogenic
ation of a sequencing library, sequencing of DNA frag- and spoilage microorganisms as well as the AMR present
ments, and mapping to known sequences to identify ARGs in fish and fish products throughout the production and
and/or mutations known to cause resistance (Schmieder supply chain. Human pathogens and spoilage microorgan-
& Edwards, 2012). Although limited studies exist in fish, isms known to cause chemical safety concerns have been
those that do exist have provided novel insights into the isolated from the fish living/rearing environment (e.g.,
ARGs and fish safety. For example, up to 80 different water and sediment) and different locations in the process-
ARGs were found in the gut microbiome of a fish called ing environment. It has been challenging to define the spe-
Piaractus mesopotamicus during oral administration of a cific contamination source in a given fish or fish product
florfenicol-medicated diet (Sáenz et al., 2019). Most of (Jami et al., 2014). Table 9 summarizes the potential con-
the ARGs were harbored by Bacteroides (25.3%), Citrobac- tamination sources of fish and fish products.
ter (20.1%), Klebsiella (9.05%), and Plesiomonas (8.29%).
An increase of MGEs, notably phage integrase and trans-
posase, co-occurred with the enrichment of ARGs. The 3.1 Preharvest
plasmid-mediated rise of ARGs during florfenicol treat-
ment also led to enrichment of the Enterobacteriaceae 3.1.1 Water
family, including the species Klebsiella and Salmonella,
which threaten the chemical and microbial safety, respec- Water has been previously reported to shape the fish micro-
tively, of fish. Another recent study detected 51 ARGs in biome (Giatsis et al., 2015; Webster, Consuegra, Hitch-
the gut microbiota of fish sampled from aquaculture farms ings, & de Leaniz, 2018; Wu et al., 2012). Unfortunately,
(Tyagi, Singh, Thammegowda, & Singh, 2019). These ARGs water is also a reservoir of contaminants in multiple layers.
belonged to 15 different AMR gene families, conferring not First, various human pathogens and spoilage microorgan-
only resistance against 24 individual drug types but MDR isms as well as ARB have been detected in water samples
as well. collected from the fish living/rearing environment. The
764
TA B L E 9 Sources of pathogenic bacteria, spoilage bacteria, antibiotic-resistant bacteria, and antibiotic-resistant genes in fish and fish products
Sources of contamination Fish and fish products Country Contaminants Reference
Preharvest
Water Freshwater fish (Gibel carp, China Aeromonas hydrophila and Li et al. (2020)
black carp, yellow catfish) Pseudomonas fluorescens
Fish China ARG Klase et al. (2019)
Salmonella
Proteobacteria, Actinobacteria,
Bacteroidetes
Seawater fish China ARG Wang et al. (2018)
Proteobacteria, Bacteroidetes
Tilapia China Proteobacteria, Cyanobacteria, Fan et al. (2016)
Bacteroidetes, Actinobacteria,
Planctomycetes, and others
Fish China ARG Xiong et al. (2015)
Proteobacteria, Actinobacteria,
Bacteroidetes, and others
Carp Poland ARB Zdanowicz et al. (2020)
Aeromonas spp.
European grayling Poland Pseudomonas fluorescens, and Golas et al. (2019)
Gilthead seabream and Spain Vibrio spp. Correia Peres Costa et al. (2020)
seabass
Fish India Aeromonas spp. Rather et al. (2019)
Freshwater fish Iran ARB Ranjbar et al. (2019)
Aeromonas spp.
Catfish USA ARG Zeng et al. (2019)
Proteobacteria, Bacteroidetes,
Actinobacteria, and
Verrucomicrobia
Rainbow trout USA Firmicutes, Proteobacteria, Betiku et al. (2018)
Bacteroidetes, and Actinobacteria
Fish (walleye, yellow perch, USA ARG Seyfried et al. (2010)
splake, trout, salmon)
Tilapia Philippines Aeromonas hydrophila, Bacillus spp., Pakingking et al. (2015)
Vibrio cholerae., Shewanella
putrefaciens, Pseudomonas
fluorescens, and others
(Continues)
Tilapia The Netherlands Proteobacteria, Actinobacteria, Giatsis et al. (2015)
Bacteroidetes, Firmicutes,
Nitrospirae, and others
Catfish and tilapia Malaysia ARB Budiati et al. (2013)
Salmonella spp.
Tropical freshwater fish Malaysia Listeria monocytogenes, Apun, Yusof, and Jugang (1999)
Staphylococcus sp., Bacillus sp.,
Aeromonas hydrophila,
Escherichia coli, and others
Carp Pakistan ARG Shah et al. (2012)
ARB
Pseudomonas spp., Acinetobacter

spp., Aeromonas hydrophila,
Enterobacter cloacae, Enterococcus
casseliflavus, and others
Tilapia Tanzania ARG Shah et al. (2012)
ARB
Proteus spp., Pseudomonas spp.,
Acinetobacter sp., Klebsiella
oxytoca, Providencia alcalifaciens,
and others
Fish Vietnam ARB Hoa et al. (2011)
Acinetobacter spp., Aeromonas spp.,
Bacillus spp., Pseudoalteromonas
spp., Pseudomonas spp., and others
Rainbow trout France ARB Naviner et al. (2011)
Aeromonas spp.
Freshwater fish Finland Listeria monocytogenes Katzav et al. (2006)
Rainbow trout Denmark Listeria monocytogenes Hansen et al. (2006)
Tilapia Saudi Arabia Vibrio spp., Chryseomonas sp., Al-Harbi and Uddin (2005)
Streptococcus sp., Aeromonas
hydrophila, Bacillus sp., and others
Freshwater Atlantic salmon Chile Pseudomonas spp., Acinetobacter Miranda and Zemelman (2002)
Escherichia coli, Morganella
morganii, and others
(Continues)
765
766

Sediment Freshwater fish (Gibel carp, China Aeromonas hydrophila and Li et al. (2020)
black carp, yellow catfish) Pseudomonas fluorescens
Fish China ARG Xiong et al. (2015)
Proteobacteria, Firmicutes,
Bacteroidetes, Actinobacteria,
Verrucomicrobia, and others
Fish China ARG Yang et al. (2013)
Proteobacteria, Firmicutes,
Actinobacteria
Grass carp China Proteobacteria, Firmicutes, Wu et al. (2012)
Fusobacteria Bacteroidetes, and
Chloroflexi
Catfish USA Aeromonas hydrophila Cai et al. (2019)
Catfish USA ARG Zeng et al. (2017)
Fish (walleye, yellow perch, USA ARG Seyfried et al. (2010)
splake, trout, salmon)
Fish (European whitefish, Finland ARG Muziasari et al. (2016)
Linnaeus, rainbow trout,
Walbaum)
Tilapia Philippines Aeromonas hydrophila, Bacillus spp., Pakingking et al. (2015)
Vibrio cholerae., Shewanella
putrefaciens, Pseudomonas
fluorescens, and others
Carp Pakistan ARG Shah et al. (2012)
ARB
Pseudomonas spp., Acinetobacter
Enterobacter cloacae, Enterococcus
casseliflavus, and others
Tilapia Tanzania ARG Shah et al. (2012)
ARB
Proteus spp., Pseudomonas spp.,
Acinetobacter sp., Klebsiella
oxytoca, Providencia alcalifaciens,
and others
Saltwater salmon Chile ARG Buschmann et al. (2012)
Rainbow trout Australia ARB Akinbowale, Peng, Grant, and
Aeromonas and Pseudomonas Barton (2007)
(Continues)
Freshwater fish Finland Listeria monocytogenes Katzav et al. (2006)
Tilapia Saudi Arabia Vibrio spp., Chryseomonas sp., Al-Harbi and Uddin (2005)
Streptococcus sp., Aeromonas
hydrophila, Bacillus sp., and others
Postharvest
Food contact surfaces Fish Poland ARB Skowron et al. (2019)
(de-heading machine, Listeria monocytogenes
skinner, slicer, scale,
cutting table, trimming

table, weighing table,
packaging equipment,
conveyor, tray, injector,
knife, box)
Fish India Listeria monocytogenes Selvaganapathi et al. (2018)
Tilapia Brazil Listeria monocytogenes Vazquez-Sanchez, Galvao, and
Oetterer (2017)
Salmon Norway Pseudomonas and Shewanella Møretrø et al. (2016)
Fish (Atlantic mackerel, Norway Listeria monocytogenes Svanevik, Roiha, Levsen, and
herring stocks, blue Lunestad (2015)
whiting, Barents Sea
capelin)
Fish and other seafood Iran ARB Fallah et al. (2013)
RTE fish Canada Listeria monocytogenes Kovacevic et al. (2012)
Cold-smoked trout Serbia Listeria monocytogenes Dimitrijevic et al. (2011)
Cold-smoked salmon Ireland Listeria monocytogenes Chitlapilly Dass, Abu-Ghannam,
Antony-Babu, and J. Cummins
(2010)
Catfish USA Listeria monocytogenes Chen et al. (2010c)
Non-food contact surfaces Smoked salmon Ireland Listeria monocytogenes Leong, Alvarez-Ordonez,
(floor, drains, walls) Zaouali, and Jordan (2015)
(Continues)
767
768
Fish (Atlantic mackerel, Norway Listeria monocytogenes Svanevik et al. (2015)
herring stocks, blue
capelin)
Salmon Norway Listeria monocytogenes Lunestad, Truong, and Lindstedt
(2013)
RTE fish Canada Listeria monocytogenes Kovacevic et al. (2012)
Catfish USA Listeria monocytogenes Chen et al. (2010c)
Personnel Tilapia Brazil Listeria monocytogenes Vazquez-Sanchez et al. (2017)
(aprons, gloves, boots)
Salmon Norway Listeria monocytogenes Lunestad et al. (2013)
Cold-smoked salmon Ireland Listeria monocytogenes Chitlapilly Dass et al. (2010)
Others Fish Poland ARB Skowron et al. (2019)
(Brine, ice, air, water) Listeria monocytogenes
Fish India ARB Divyashree et al. (2019)
ARG
Proteus spp., Pseudomonas spp., E.
coli spp., Aeromonas spp.,
Salmonella spp., and others
Salmon Norway Pseudomonas, Shewanella, and Møretrø et al. (2016)
Photobacterium
Fish (Atlantic mackerel, Norway Listeria monocytogenes Svanevik et al. (2015)
herring stocks, blue
capelin)
Abbreviations: ARB, antimicrobial-resistant bacteria.; ARG, antibiotic-resistant genes; NA, not available; RTE, ready-to-eat.
reported ARB include Salmonella spp., Aeromonas spp., no significant differences in ARB prevalence between the
Acinetobacter spp., Pseudomonas spp., Bacillus spp., Pseu- two seasons when the fish pond water was sampled, indi-
doalteromonas spp., Proteus spp., and many others (Budiati cating that the fish pond water was less affected by the
et al., 2013; Hoa et al., 2011; Naviner et al., 2011; Ranjbar, rainfall.
Salighehzadeh, & Sharifiyazdi, 2019; Shah, Colquhoun,
Nikuli, & Sorum, 2012; Zdanowicz, Mudryk, & Perlin-
ski, 2020). Furthermore, ARGs were detected in water 3.1.2 Sediment
microbiota using culture-independent methods, for exam-
ple, quantitative PCR (qPCR) and shotgun metagenomic Compared to water, sediment harbors higher numbers
sequencing (Klase et al., 2019; Seyfried, Newton, Rubert, and diversities of bacteria and antibiotic residues (Al-
Pedersen, & McMahon, 2010; Shah et al., 2012; Wang et al., Harbi & Uddin, 2005; Li et al., 2020; Zeng, Tian, & Wang,
2018; Xiong et al., 2015; Zeng, Liao, Terhune, & Wang, 2017). Xiong et al. (2015) reported that although the
2019). Last but not least, MGEs, which can transfer ARGs concentrations of sulfametoxydiazine, sulfamethazine,
to other bacteria in fish and the environment, have also sulfamethoxazole, oxytetracycline, chlorotetracycline,
been isolated from water microbiota (Budiati et al., 2013; doxycycline, ciprofloxacin, norfloxacin, and enrofloxacin
Ranjbar et al., 2019). For example, L. monocytogenes has varied from undetectable to 446 μg/kg in sediment, the
been isolated from fish-farm water in Finland and Den- antibiotic residue concentrations in water ranged from
mark (Hansen, Vogel, & Gram, 2006; Katzav, Hyvonen, undetectable to 98.6 μg/kg. Rearing sediment is reported
Muje, Rantala, & Von Wright, 2006). A recent study by to typify fish microbiota (Pakingking, Palma, & Usero,
Klase et al. (2019) detected Salmonella in 37% of fish-farm 2015). Human pathogens, spoilage microorganisms, and
water in China. They also found ARGs targeting for tetra- ARGs, as well as MGEs, have all been detected in sediment
cycline, sulfonamide, and carbapenem resistance in all collected from the living environment of fish. For example,
water samples. Budiati et al. (2013) found that Salmonella A. hydrophila has been isolated from 22.9% of sediment
spp. in the water of catfish and tilapia were not only resis- samples in catfish production ponds in the United States,
tant to antibiotics but harbored plasmids carrying ARGs. whereas the pathogen was not in any of the water samples
Aeromonas spp. resistant to multiple antibiotics was recov- collected (Cai et al., 2019). Salmonella, Clostridium, L.
ered from fish-farm water in Iran (Ranjbar et al., 2019). monocytogenes, and Escherichia/Shigella have also been
Of those resistant isolates, 15% contained class 1 integrons, detected in the sediment from fish ponds (Katzav et al.,
which contain seven types of integron cassette arrays and 2006; Xiong et al., 2015). A study of marine aquaculture
are proven to transport different ARG cassettes. Wang et al. in China extracted plasmids from fish-farm sediments
(2018) found 21 ARG types in coastal industrial maricul- and sequenced the plasmid metagenome (Yang et al.,
ture water using shotgun metagenomics; Proteobacteria 2013). From these samples, the authors identified 58 genes
and Bacteroidetes showed the highest co-occurrence with with high homology conferring resistance to 11 antibiotic
ARGs, suggesting they were the dominant hosts. classes. Additionally, six ARG-carrying contigs were
The microbiota of water is influenced by many factors, found that had more than 90% identity to transposons or
including water’s physiochemical properties, the seasons, plasmids of human pathogens, indicating the potential of
and climate conditions. The occurrence of A. hydrophila resistance genes exchange between sediment microbiota
and P. fluorescens in water collected from freshwater fish and human pathogens.
ponds had a significant positive correlation with water The occurrence of contaminants in sediment is influ-
temperature and dissolved oxygen, and a negative corre- enced by sampling times (seasons) and sampling locations.
lation with total nitrogen (Li, Zhu, Ringø, & Yang, 2020). For example, Cai et al. (2019) collected fish-pond sedi-
Aeromonas spp. showed a significant seasonal change in ment samples from three commercial catfish farms in the
water from carp ponds, with summer having the highest U.S. state of Alabama monthly from July to October. The
and fall having the lowest levels (Zdanowicz et al., 2020). incidence of A. hydrophila in August was 41.7%, followed
Hansen et al. (2006) did not find significant seasonal vari- by 25% in September and October. Aeromonas hydrophila
ations of L. monocytogenes in water from freshwater fish was absent in the July sediment samples. Buschmann
farms in summer and winter. Climate conditions, partic- et al. (2012) compared the prevalence of culturable ARB to
ularly rainfall, are reported to contribute to bacterial con- oxytetracycline, oxolinic acid, and florfenicol in sediment
tamination of surface water (Jami et al., 2014). Hoa et al. samples with varying distances from an aquaculture site in
(2011) found a higher occurrence of ARB in a city canal Chile. There was no significant difference in the incidence
during the high rainfall season (July, 286 mm of rain- of ARB in sediments collected within 1 km of the aqua-
fall monthly) than during the dry season (January, 2 mm culture site, which was significantly higher than the inci-
of rainfall monthly). In the same study, the team found dence of ARB in sediments collected 8 km away, where had
been no observable aquaculture activities. Interestingly, Besides direct antibiotic treatments, application of live-
ARGs were detected at similar frequencies in all sampling stock waste in fish farms can also indirectly introduce
sites, indicating that aquaculture activities might spread antibiotics to the aquaculture system. Integrated fish farm-
ARGs to the surrounding environment. Similarly, Muzi- ing is a common practice among small-scale fish farms
asari et al. (2016) detected ARGs and transposase genes in in Asia and Africa, where livestock waste (manure and
sediment samples collected from both a fish farm and the urine) is administered to fish ponds as fertilizers, feeds, or
surrounding environment using high parallel qPCR. These substrates to produce live feeds (Little & Edwards, 1999).
results demonstrated that aquaculture practices, particu- Livestock manure is known to harbor various human
larly practices in open systems where both uneaten fish pathogens (Hutchison, Walters, Avery, Munro, & Moore,
feed and fish excrement transfer freely, can pose risks to the 2005), antibiotic residues (Zhao, Dong, & Wang, 2010),
surrounding environment, and these practices can directly ARB, and various ARGs (He et al., 2020). Livestock waste
impact the diversity and abundance of the microbial con- application has been reported to modulate the micro-
taminants present in the sediment. biomes and resistomes of water and sediment in the
aquaculture environment. For example, the prevalence of
antibiotic-resistant Acinetobacter spp. in water and sed-
3.1.3 Influence of antibiotics usage iment samples increased with the increase of produc-
tion time in chicken–fish ponds in Thailand (Petersen,
Diseased fish can spread their pathogenic microbiota to the Andersen, Kaewmak, Somsiri, & Dalsgaard, 2002). ARGs
surrounding environment and transmit disease to farmed encoding tetracycline, trimethoprim, amoxicillin, strepto-
or wild fish (Behbahani, Akhlaghi, & Sharifiyazdi, 2014; mycin, chloramphenicol, and erythromycin were detected
Munn, 2019; Zhou et al., 2013). Antibiotics are widely used in water, sediment, and fish samples collected from inte-
in aquaculture to prevent diseases and promote growth grated fish farming systems in Pakistan and Tanzania with
of fish. Globally, the most commonly used antibiotics no history of antibiotic use (Shah et al., 2012).
in aquaculture are oxytetracycline and chloramphenicol, In addition, heavy metals, which are frequently used
which belong to the antibiotic category of tetracycline, as in aquaculture to provide nutrients or treat infections,
well as oxolinic acid from the quinolones category (Sapkota can trigger co-selection of ARGs in the rearing environ-
et al., 2008). Antibiotics are mostly administered to fish ment when critical concentrations of heavy metals are
through feeds (Cabello et al., 2013). The unconsumed med- reached (Seiler & Berendonk, 2012). A recent study found
icated feed as well as fish excrement containing ingested that manganese (Mn) and zinc (Zn) were positively cor-
antibiotics both contribute to the leaking of antibiotics into related with most ARGs and four sulfonamides includ-
the rearing environment (Muziasari et al., 2016, 2017; Zeng ing sulfapyridine, sulfadiazine, trimethoprim, and sul-
et al., 2017). The prolonged usage of antibiotics adds selec- famethoxazole in aquaculture sediments in China (Lu
tive pressure to microbiota in aquaculture and modulates et al., 2020). The selected ARGs are highly persistent in the
the microbiomes of water and sediment, as well as their environment. Tamminen et al. (2011) detected tetracycline-
resistome, which is defined as “a collection of all ARGs resistant genes in the sediment samples of a rainbow trout
and their precursors in pathogenic and nonpathogenic and common whitefish farm in Finland for four con-
bacteria” (Wright, 2007). Zeng et al. (2019) conducted a secutive years, even though the farm had stopped using
metagenomic analysis of water in enclosed catfish tanks any antibiotic 6 years prior to the first sampling, and no
in the United States and found that florfenicol treatment therapeutically active concentrations of tetracycline were
reduced the overall biodiversity in water while increas- detected in any sample. In the study conducted by Muzi-
ing the abundance of bacteria belonging to Proteobac- asari et al. (2014), ARGs for sulfoamides and trimethoprim
teria, Bacteroidetes, Actinobacteria, and Verrucomicro- were found to persist in fish-farm sediments for 6 years.
bia, which coincided with expanded florfenicol-resistant Several other reviews have also discussed the influence
genes. The resistance was achieved through both hori- on fish and human health of antibiotics usage in aqua-
zontal gene transfer and mutation. Muziasari et al. (2016) culture (Cabello et al., 2013; Heuer et al., 2009; Ibrahim
found that fish-farm sediment resistomes were enriched et al., 2020; Lulijwa, Rupia, & Alfaro, 2020; Okocha, Ola-
in ARGs encoding resistance to tetracycline, sulfonamide, toye, & Adedeji, 2018; Preena et al., 2020; Sapkota et al.,
and trimethoprim, which were used in these fish farms in 2008; Watts et al., 2017). Overall, the use of antimicro-
the past. The ARG profile of sediments collected from two bials, livestock waste, and heavy metals needs to be bet-
fish farms was similar, although the farms were separated ter investigated to prevent the formation and persistence
by tens of kilometers geographically while having a similar of pathogens, ARB, and ARGs in aquaculture production
history of antibiotic usage. systems.
3.1.4 Other preharvest factors els; and temperature abuse during transportation and in
the supply chain. The following discussion will focus on
Other preharvest factors can impact and contribute to these two areas.
the abundance and composition of microbial populations With human pathogens remaining a challenge in fish
present in the final fish product, including intrinsic fac- processing plants, other contaminants that pose safety
tors (e.g., genetics) and extrinsic factors (e.g., water sources risks, including ARB and ARGs, as well as spoilage
and routine aquaculture practices), all of which have been microorganisms, have all been detected in processing
extensively reviewed previously (Beck & Peatman, 2015; plants and have received increasing attention. Fallah et al.
Butt & Volkoff, 2019; Ghanbari, Kneifel, & Domig, 2015; (2013) found that approximately 81% of 278 L. monocy-
Legrand et al., 2019; Ringø et al., 2016; Talwar, Nagar, Lal, togenes isolates recovered from the fish processing envi-
& Negi, 2018; Yukgehnaish et al., 2020). Most of these ronment, personnel, and fish and other seafood in Iran
previous reviews have focused on fish gut microbiomes were resistant to antibiotics. More than 22% of the iso-
due to their unique and significant impacts on the nutri- lates demonstrated MDR. Skowron et al. (2019) reported
tion, health, and general well-being of fish as well as that antibiotic-resistant L. monocytogenes was present in
their involvement in the shelf-life and spoilage of fish 40% of isolates from fish processing plants in Poland;
products. As reviewed by Ringø et al. (2016), the fish gut one strain showed MDR against penicillin, ampicillin, and
microbiome is impacted and determined by many factors, erythromycin. Divyashree et al. (2019) examined the cul-
including dietary manipulations, seasons, stresses, indi- turable microbiota, AMR, and ARGs in untreated efflu-
vidual variations, production and harvest methods (cul- ent samples from the drainage system at fish processing
tured vs. wild), triploid versus diploid, day-to-day varia- plants. They isolated 179 Gram-negative bacteria, includ-
tions, genders, developmental stages and life cycles, feed, ing Proteus spp. (30.72%), E. coli (17.31%), Pseudomonas spp.
growing status and speed, hierarchy formation, water qual- (12.84%), Aeromonas spp. (8.93%), Citrobacter spp. (8.83%),
ity (e.g., recirculation vs. conventional flow-through), and Enterobacter spp. (6.14%), Salmonella spp. (6.14%), Vibrio
other farming, environmental, and ecological factors. spp. (3.91%), Shigella spp. (2.23%), Klebsiella spp. (1.67%),
and Morganella spp. (1.11%). More than 40% of the isolates
were resistant to ampicillin or tetracycline, and 23.46%
3.2 Postharvest of them were multidrug resistant. ARGs conferring resis-
tance to tetracycline and sulfonamides have also been
Numerous postharvest processing and handling practices detected from these isolates. Møretrø, Moen, Heir, Hansen,
collectively play an important role in fish product safety. As and Langsrud (2016) evaluated the microbial populations
summarized in Table 9, postharvest contamination sources in salmon processing plants, and the authors found that
include fish contact surfaces (e.g., slicer, conveyor belt, 49% to 62% of samples collected from equipment (e.g.,
and knife), nonfish contact surfaces (e.g., floor, drain, and stunning machine, head cutter, gutting machine, filleting
wall), personnel (e.g., aprons, gloves, and boots), and oth- machine, trimming machine, bone remover, and conveyor
ers (e.g., air, ice, and water). Most of the studies focused systems) were positive for Pseudomonas, followed by 18% to
on human pathogens in fish processing facilities, which 26% positive for Shewanella. These results showed that pro-
are considered the main source for introducing pathogens cessing plants and equipment and utensils are important
into fish and fish products (Fernandes et al., 2018). In par- sources for spoilage microorganisms, AMR, and ARGs.
ticular, L. monocytogenes has been extensively screened Besides contamination in fish processing facilities,
due to its ubiquity in the environment and ability to pro- contamination at the consumer and restaurant levels has
liferate at cold temperatures, as well as significant safety gained increasing attention. Cross-contamination and
consequences on human health. Jami et al. (2014) have bacterial growth are the two major concerns. Hands and
reviewed the contamination sources of L. monocytogenes utensils, as well as other food contact surfaces in kitchens,
in seafood processing environments from 1999 to 2012 in have repeatedly been reported as contamination sources
great detail. Fernandes et al. (2018) discussed the con- based on several recent studies (Dantas et al., 2018; Habib
tamination of fish and fish products with Salmonella in et al., 2020; Rossi, Beilke, & Barreto, 2018; Sekoai et al.,
the fish production chain. They suggested that biofilm 2020). Poor food handling and hygiene practices further
formation and inadequate sanitation contribute to the increase the risk of cross-contamination. A survey study
cross-contamination of human pathogens. In recent years, conducted in Turkey showed that more than 45% of
greater attention has been paid to the prevalence and per- consumers reported using the same equipment for raw
sistence of ARB, ARGs, MDR, and spoilage microorgan- and cooked fish (Mol, Akay, & Guney, 2018). Over 60% of
isms in the postharvest environment; contamination and people cleaned kitchen surfaces only at the end of the day.
cross-contamination at the consumer and restaurant lev- In a U.S. survey among families with young children, 93%
of food preparers said they never put cooked meat on the Nile tilapia challenged with A. hydrophila after 30 days of
same plate where raw meat has been, but only 37% declared feeding. The survival rate of fish increased from about 36%
that they always separate raw meat from other food in the for untreated fish to 54 and 46% for fish fed with 2.22 g
grocery cart (Lum, Albrecht, Yaseen, Litchfield, & Ritter- propolis ethanolic extract/kg of feed and 0.5% oregano
Gooder, 2013). Once pathogenic or spoilage microorgan- oil/feed, respectively, after 15 days of infection.
isms are introduced into fish and fish products, regardless In the postharvest stage, intervention strategies are
of the contamination routes, they have the potential to pro- developed and implemented with the goals of (a) reducing
liferate to high levels during transportation, storage, and or eliminating pathogenic and spoilage microorganisms
handling, particularly under temperature abuse condi- in fish products before storage and (a) controlling micro-
tions. Unfortunately, temperature fluctuation can happen bial growth during distribution, storage, and handling of
throughout the supply chain. Temperature increase of fish products. Most of the novel processing methods are
fish by 2 ◦ C or higher has been reported during both land nonthermal in order to retain the nutrition value and sen-
and air transportation (Abad et al., 2009). During storage, sory attributes of fish. Mild thermal processing coupled
the ideal temperatures for frozen and chilled fish and fish with antimicrobials has also been suggested (Ovissipour,
products are −18 ◦ C (or lower) and –0.5 to 0 ◦ C (in melting Shiroodi, Rasco, Tang, & Sablani, 2018; Shiroodi, Ovis-
ice), respectively (Mercier, Villeneuve, Mondor, & Uysal, sipour, Ross, & Rasco, 2016). These methods also are envi-
2017). However, a survey study of 200 home refrigerators ronmentally friendly and more energy efficient. DeWitt
in the United States showed that temperatures of 13.3% of and Oliveira (2016) discussed the application of MAP to
doors and 3.7% of bottom shelves are higher than 7.3 ◦ C extend the shelf life of fish and fish products as well as
(Godwin, Chen, IV, Coppings, & Chambers, 2007). More the detailed fish handling and quality guidelines to max-
than 40% of food preparers reported leaving fresh or frozen imize the beneficial effects of MAP. Olatunde and Ben-
fish/meat on the counter during fish handling (Baptista, jakul (2018) reviewed some nonthermal processes includ-
Rodrigues, & Sant’Ana, 2020; Lum et al., 2013; Mol et al., ing chemical pretreatments such as acidic electrolyte water
2018). Increasing food handlers’ knowledge and awareness and ozone washing, and physical processing technologies
of food safety practices is essential to make fish handling such as pulsed electric field, high hydrostatic pressure,
safer and improve the safety of fish and fish products. cold plasma, ultraviolet, MAP, and irradiation. The authors
discussed the principle, antimicrobial efficacy, and appli-
cation, as well as limitations of these nonthermal pro-
4 INTERVENTION STRATEGIES cesses, in detail. Most of these previous studies and reviews
focused on the reduction of pathogenic and spoilage bacte-
Intervention strategies are applied at both pre- and rial counts, production of volatile compounds, and sensory
postharvest stages to reduce the incidence of the afore- characteristics. However, information about unculturable
mentioned contaminants (ARB, ARGs, human pathogens, microorganisms, which account for the majority of fish
and spoilage microorganisms), improving product safety microbiota and play an important role in fish and fish prod-
and extending product shelf life. During the preharvest ucts safety, is limited and warrants more attention. With
stage, alternatives to antibiotics for treating diseases the help of NGS, more insights into the bacterial composi-
or promoting the growth of fish have been suggested, tion and dynamics of fish and fish products will contribute
including prebiotics; synbiotics; probiotics; medici- to a better understanding of the efficacy of interventions
nal plants; plant, herbal, algal, and fungal extracts; as well as the development of target-specific intervention
pathogen-associated molecular patterns (beta-glucan, strategies. The following part will focus on recent findings
Saccharomyces cerevisiae, chitin); and vaccines (Hoseini- about the influence of novel nonthermal processes on the
far, Sun, & Zhou, 2017; Reverter, Tapissier-Bontemps, bacterial microbiome of fish and fish products using NGS.
Sasal, & Saulnier, 2017; Sharifuzzaman & Austin, 2017; Nonthermal processes can be classified into two main
Vallejos-Vidal, Reyes-López, & MacKenzie, 2017). For groups: physical and chemical interventions. Physical pro-
example, a recent challenge study reported that diets cesses are reported to effectively reduce the abundance and
supplemented with Bacillus spp. significantly increased diversity of fish spoilage microbiota. Tsironi et al. (2019)
resistance to A. hydrophila infection in Nile tilapia (Kueb- applied 600 MPa high-pressure treatment at 25 ◦ C for 5 min
utornye et al., 2020). The cumulative mortality rate 7 days on European seabass fillets and found that this treatment
postchallenge with A. hydrophila was reduced from 87% extended the shelf life from 11 days to 2 months. The 16S
for control fish to 30% for tilapia fed with a diet containing rRNA sequencing results showed that high-pressure pro-
Bacillus velezensis, Bacillus subtilis, and Bacillus amyloliq- cessing (HPP) markedly reduced the relative abundance
uefaciens. de Oliveira et al. (2020) investigated the use of of Shewanella and suppressed the growth of Aeromonas
oregano oil and propolis extracts as functional foods for during subsequent cold storages at 2 ◦ C. Kuuliala et al.
(2018) evaluated the composition of the microbiota of 0.1% (v/v) essential oil solutions for 30 min at room temper-
Atlantic cod fillets during 4 ◦ C storage in air and dif- ature prior to packaging and storage extended the shelf life
ferent MAP conditions. After 3 days, the microbiota of of fish fillets by 2 days. In general, essential oil treatments
the air-stored cod was dominated by Photobacterium, reduced the relative abundance of Aeromonas and She-
Acinetobacter, Pseudomonas, and Psychrobacter, whereas wanella during storage. This group also studied the influ-
Photobacterium was the only dominant genus in those ence of chitosan (Jia et al., 2018), pomegranate peel extract
stored for 5 days in 60% CO2 , 5% O2 , and 35% N2 . Besides (Zhuang et al., 2019), tea polyphenols (Jia et al., 2018), and
the aforementioned physical interventions, photodynamic cinnamon bark oil (Huang, Liu, Jia, & Luo, 2017) on the
inactivation of bacteria (PIB) has gained increasing popu- spoilage microbiome dynamics in fish fillets during stor-
larity to control microbiological food safety (Ghate, Zhou, age.
& Yuk, 2019). The principle of PIB starts with light absorp- Besides single intervention strategies, the combination
tion by a photosensitizer, energy transfer to a substrate of different methods (also known as hurdle technology)
or molecular oxygen, and the formation of highly toxic has been widely studied to ensure fish and fish products
reactive oxygen species (Fang, 2004; Foote, 1991). There safety. This utilizes a combination of different antimicro-
are several factors impacting the efficacy of photodynamic bial mechanisms to achieve a better preservation. Chen
inactivation, including intrinsic factors and extrinsic fac- et al. (2020) reported 6% salt and vacuum packaging
tors. Intrinsic factors are associated with food itself, such together extended the shelf life of Russian sturgeon dur-
as the acidity, surface properties, water activity, available ing storage at 4 ◦ C by delaying the growth of Pseudomonas.
nutrients, and presence of potential natural antagonism Sørensen et al. (2020) examined the combination of super-
microorganisms. Extrinsic factors include environmental chilling and MAP on the microbial quality of Atlantic cod.
factors (e.g., storage or treatment temperatures and the Under regular air storage on ice, the shelf life was 15 days,
availability of oxygen) and engineering factors (such as whereas superchilling at –1.7 ◦ C and MAP storage with
the wavelength and dose). So far, PIB has been applied 40% CO2 and 60% N2 extended the shelf life to more than
onto products such as fruit, meat, and grain, as well as 32 days. The bacterial communities of iced cod in air at
food contact surfaces (Ghate et al., 2019; Sheng, Zhang, shelf life were dominated by Pseudomonas (36.2%), Pho-
Sun, & Wang, 2020). Although no direct application has tobacterium (24.1%), Shewanella (15.5%), and Acinetobac-
been made to fish or fish products so far, the efficacy of ter (14%). The microbiota of superchilled cod in MAP by
PIB over both pathogens and spoilage bacteria indicates the end of 32 days of storage mainly consisted of Photo-
promising potential applications in fish and fish products bacterium (40.5%), Pseudomonas (31.6%), and Acinetobac-
or fish processing equipment. ter (12.5%).
Due to the safety concerns about synthetic chemicals, After processing and manufacturing, it is also impor-
application of natural chemical preservatives to fish and tant to ensure proper distribution, storage, and handling
fish products has been on the rise. Antimicrobial ingre- of fish products to prevent cross-contamination or micro-
dients, plant extracts, and essential oils have been shown bial growth during the latter part of the supply chain.
to modulate the spoilage microbiota composition and Time and temperature abuse contributes to up to 53.8%
dynamics of fish and fish products. For example, salt of foodborne-illness outbreaks, followed by improper food
and sugar are added to fish and fish products not only storage (0 to 27.9%) and cross-contamination (0 to 24.6%)
to improve the flavor and taste but to prolong shelf life (Todd, Greig, Bartleson, & Michaels, 2007). The cold chain,
through the reduction of water activity. After 8 days of a controlled temperature supply chain, denotes the equip-
storage at 4 ◦ C, the bacterial communities in blunt snout ment and management used to maintain chilled and
bream fillets that had been slightly salted with 1.8% salt frozen perishable foods in the desired temperature range
consisted of 34% Pseudomonas, 28% Pseudoalteromonas, from production to consumption (Montanari, 2008). Good
20% Shewanella, and 8% Psychrobacter, compared to 65% cold chain management can not only ensure fish and
Pseudomonas, 20% Shewanella, 8% Aeromonas, and 5% fish products safety but also reduce food waste. Mercier
Acinetobacter in unsalted control fillets (Li et al., 2018). The et al. (2017) reviewed current cold chain management
addition of sugar further changed the relative abundance and identified several steps prone to temperature abuse,
of different spoilage microbiota. After 8 days of storage, the including precooling, ground operations during trans-
1.8% salt- and 0.9% sugar-treated fish fillets contained 46% portation, retail display, and domestic refrigeration. Cold
Pseudomonas, 17% Shewanella, 15% Pseudoalteromonas, chain management is further complicated by the product-
9% Psychrobacter, and 7% Acinetobacter. Huang, Liu, Jia, dependent requirements of storage temperature. Improve-
Zhang, and Luo (2018) evaluated oregano, thyme, and star ment of time–temperature management in the cold chain,
anise essential oils on the microbial composition and qual- a widespread implementation of cold chain management
ity of grass carp fillets during storage at 4 ◦ C. Immersion in as well as better food safety knowledge and behavior
among consumers will contribute to the control of fish and warehouses to identify and avoid physical, chemical, and
fish products safety. biological hazards that have the potential to cause food-
borne illnesses (Tom, 2012). FDA also recently released the
fourth edition of its Fish and Fishery Products Hazards
5 GOVERNMENT REGULATIONS and Controls guidance to assist fish and fishery products
processors in developing their HACCP plans (FDA, 2020b).
Regulations have been established to provide guidance For the final fish products, FDA and the U.S. Envi-
documents for good farming and processing practices. The ronmental Protection Agency (EPA) have regulations and
global harmonization of laws, regulations, and manufac- guidance about the safety levels of animal drugs, bio-
turing/storage/packaging practices is the key to ensur- logical agents, chemicals, and toxins, as well as physi-
ing the microbial safety of fish and fish products. The cal hazards (FDA, 2020b). For example, no residues of
approved antibiotics for use in aquaculture vary among chloramphenicol, clenbuterol, diethylstilbestrol, dimetri-
different countries (Preena et al., 2020). For example, dazole, furazolidone, fluoroquinolones, or glycopeptides
China, the leading aquaculture producer globally, autho- are permitted in any fish (21 CFR 530.41). The tolerance
rized 13 antibiotics for aquaculture usage, including doxy- for the sum of tetracycline (oxytetracycline, chlortetracy-
cycline, enrofloxacin, florfenicol, flumequine, neomycin, cline, and tetracycline) residues in finfish muscle is 2 ppm
norfloxacin, oxolinic acid, sulfadiazine, sulfamethazine, (21 CFR 556.500). Residues of florfenicol should be less
sulfamethoxazole, sulfamonomethoxine, thiamphenicol, than 1 ppm in catfish muscle tissue or the muscle/skin
and trimethoprim (Liu, Steele, & Meng, 2017). In the of freshwater-reared warm-water finfish (other than cat-
United States, the aquaculture drugs approved by FDA fish) and salmonids (21 CFR 556.283). Tolerances for sul-
include chloramine-T, formalin, hydrogen peroxide, oxyte- fadimethoxine are 0.1 ppm in edible tissues of catfish and
tracycline hydrochloride, and tricaine methanesulfonate salmonids (21 CFR 556.640), and no sulfamerazine residue
for immersion; chorionic gonadotropin for injection; is permitted in trout (21 CFR 556.660). In terms of biolog-
and florfenicol, oxytetracycline dihydrate, sulfadimethox- ical hazards, Salmonella spp. should be absent in all fish
ine/ormetoprim, and sulfamerazine fish grade for med- analyzed according to the Bacteriological Analytical Man-
icated articles/feeds (FDA, 2020a). Among the 11 major ual (CPG Sec 555.300). RTE fish products are considered
aquaculture-producing countries worldwide, 73% applied adulterated if L. monocytogenes is present in one or more
oxytetracycline, florfenicol, and sulfadiazine for growth subsamples (CPG Sec 555.320). For chemicals and toxins
promotion and/or prevention/treatment of diseases (Luli- frequently involved in fish-associated outbreaks, the pres-
jwa et al., 2020). ence of 500 ppm or higher of histamine in scombrotoxin-
For processing, the U.S. FDA regulates seafood, includ- forming fish such as tuna and mahi mahi is considered
ing fish (except Siluriformes) and shellfish under the dangerous to human health (CPG Sec 540.525). Histamine
Federal Food, Drug, and Cosmetic Act (FD&C Act) (FDA, at 50 ppm or higher is an indication of fish decomposition
2018). Domestic production and all imports of Siluriformes regardless of the organoleptic examination. It is suggested
fish and fish products, including catfish, are regulated by that the threshold level for ciguatoxin contamination is 0.1
the USDA’s Food Safety Inspection Service (FSIS) under ppb Caribbean ciguatoxin-1 equivalents in Caribbean fish
the Federal Meat Inspection Act (USDA-FSIS, 2018). FDA and 0.1 ppb Pacific ciguatoxin-1 equivalents in Pacific fish
passed its final regulation to ensure the safety and sanitary (Dickey & Plakas, 2010). Efforts have been made to harmo-
processing of fish and fish products, entitled “Procedures nize the maximum residue levels (MRLs) worldwide; how-
for the Safe and Sanitary Processing and Importing of Fish ever, MRLs vary among developed countries, whereas most
and Fishery Products,” in 1995 (FDA, 1995). This guidance developing counties do not have their own MRLs (Okocha
includes the Seafood HACCP Regulation (21CFR 123) et al., 2018). For example, the MRL for the sum of tetracy-
and Control of Communicable Disease (21 CFR 1240). cline in finfish muscle is 100 μg/kg (0.1 ppm) in the Com-
Siluriformes fish and fish products must comply with mission Regulation (EU) No 37/2010 (EU, 2010), compared
Sanitation Performance Standards, Sanitation Standard to a 2 ppm tolerance in the United States and 200 μg/kg
Operating Procedure, and the HACCP requirements (applied only to oxytetracycline) in the Codex Alimentar-
specified in 9 CFR 416 and 417 (USDA-FSIS, 2017). HACCP ius International Food Standards (FAO/WHO, 2018).
consists of seven principles, including conducting a
hazard analysis, identification of critical control points
(CCP), establishment of critical limits for each CCP, CCP 6 CONCLUSION
monitoring procedures, corrective actions, verification
procedures, and record-keeping procedures (Tom, 2012). Fish plays an important role in human diet; the production
This regulation requires fish processors, re-packers, and and consumption of fish and fish products have increased
worldwide over the years. However, fish and fish prod- imported (NOAA, 2020). In the United States, FDA spec-
ucts have been involved in various foodborne outbreaks ifies the antimicrobials approved to treat fish diseases in
and recalls annually. Microorganisms play significant roles aquaculture. Both FDA and USDA require fish processors
in fish and fish product safety. The transfer and persis- to implement a HACCP plan addressing all potential haz-
tence of human pathogens in fish and fish products and ards during processing. For finished products, FDA and
the formation of chemical hazards caused by the growth of EPA also have detailed regulations and guidance for each
spoilage microorganisms are major concerns. This review hazard. However, different countries have different reg-
aims to comprehensively dissect this issue by provid- ulations. To ensure the sustainability of global aquacul-
ing updated information about the major safety prob- ture and the availability of fish and fish products, greater
lems, identifying contamination sources, and discussing effort is still needed to harmonize regulations for both pre-
recent advancements made in intervention strategies for harvest farming practices and postharvest processing and
the control of fish and fish product safety throughout handling.
the production and supply chain. Analysis of outbreak
and recall surveillance data from CDC, FDA, and USDA AU T H O R CO N T R I B U T I O N S
shows that both human pathogens and spoilage bacte- Luxin Wang conceptualized the idea. Lina Sheng and
ria capable of elevating histamine levels are the biggest Luxin Wang planned and designed the structure of the
threats to fish and fish products safety. The emergence review. Lina Sheng wrote the manuscript. Luxin Wang
and spread of antibiotic-resistant isolates and ARGs have reviewed and edited the manuscript.
been increasing concerns for the aquaculture industry.
Prudent use of antibiotics and good fish farming prac- CONFLICTS OF INTEREST
tices are crucial for the control of ARB and ARGs. High The authors declare no conflicts of interest.
water activity, high postmortem pH (>6), and the pres-
ence of large amounts of low-molecular-weight compo- ORCID
nents make processed fresh fish fillets an ideal media for Luxin Wang https://orcid.org/0000-0003-4959-6477
bacterial growth. Inoculation studies showed that once
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Received: 2 July 2020 Revised: 22 September 2020 Accepted: 12 October 2020

COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

The microbial safety of fish and fish products: Recent

Lina Sheng Luxin Wang

Department of Food Science and

738 wileyonlinelibrary.com/journal/crf3 Compr Rev Food Sci Food Saf. 2021;20:738–786.

1 INTRODUCTION 2015; Novoslavskij et al., 2016). It is well accepted

freshwater fish chloramphenicol (30.8),

Pathogen Domestic Imported Incidence isolates (%) Reference

−20 ◦ C, plastic bag 12 months 4.4 3.7 Log CFU/g

sequencing (shotgun) of all (meta) microbial genomes 3 CONTAMINATION SOURCES

Pseudomonas spp., Acinetobacter

Sources of contamination Fish and fish products Country Contaminants Reference

cutting table, trimming

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