Journal of Infection and Public Health (2016) 9, 535—544

REVIEW

Antimicrobial resistance of Aeromonas

hydrophila isolated from different food
sources: A mini-review
Deyan Stratev a,∗, Olumide A. Odeyemi b,c

a Department of Food Hygiene and Control, Veterinary Legislation and Management,

Faculty of Veterinary Medicine, Stara Zagora, Bulgaria
b Ecology and Biodiversity, Institute for Marine and Antarctic Studies, University of

Tasmania, Australia
c ACeFORE International, Nigeria

Received 10 June 2015 ; received in revised form 3 August 2015; accepted 7 October 2015

KEYWORDS Summary Aeromonas hydrophila is a Gram-negative, oxidase-positive, faculta-

A. hydrophila; tive, anaerobic, opportunistic aquatic pathogen. A. hydrophila produces virulence
Antimicrobial factors, such as hemolysins, aerolysins, adhesins, enterotoxins, phospholipase and
resistance; lipase. In addition to isolation from aquatic sources, A. hydrophila has been isolated
Microbial food safety from meat and meat products, milk and dairy products, and vegetables. However,
various studies showed that this opportunistic pathogen is resistant to commercial
antibiotics. This is attributed to factors such as the indiscriminate use of antibiotics
in aquaculture, plasmids or horizontal gene transfer. In this report, we highlight
the occurrence, prevalence and antimicrobial resistance of A. hydrophila isolated
from different food samples. The presence of antimicrobial-resistant A. hydrophila
in food poses threats to public and aquatic animal health.
© 2015 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier
Limited. All rights reserved.

Contents

Introduction...................................................................................................536
Antimicrobial resistance of A. hydrophila in different foods...................................................536
Seafood...................................................................................................536
Meat and meat products .................................................................................. 537

∗ Corresponding author. Tel.: +359 42 699 537.

E-mail address: deyan.stratev@trakia-uni.bg (D. Stratev).

http://dx.doi.org/10.1016/j.jiph.2015.10.006
1876-0341/© 2015 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Limited. All rights reserved.
536 D. Stratev, O.A. Odeyemi

Milk and dairy products ................................................................................... 537

Vegetables................................................................................................537
Antimicrobial resistance mechanisms of A. hydrophila ........................................................ 537
Public health significance of antibiotic-resistant A. hydrophila ................................................ 540
Conclusion .................................................................................................... 541
Funding ....................................................................................................... 542
Competing interests...........................................................................................542
Ethical approval...............................................................................................542
References .................................................................................................... 542

Introduction and second- and third-generation cephalosporins

The genus Aeromonas consists of oxidase-positive,
facultative, anaerobic Gram-negative bacteria that
normally inhabit the aquatic environment. Depend-
ing on the physiological properties and hosts,
they are divided into two large groups. The first
group includes motile aeromonads, with Aeromonas
hydrophila as a typical representative that causes
infections mainly in humans. The other group
consists of non-motile species, represented by
Aeromonas salmonicida, causing disease in fish [1].
Aeromonads have been isolated from a variety
of foods, such as fish, mussels, shrimps, meat,
meat products, milk and vegetables, with total
counts ranging from 102 cfu/g to 105 cfu/g. Motile
aeromonads produce virulence factors at vary-
ing growth temperatures [2]. The presence of
Aeromonads has been reported in dairy products
(4%), vegetables (26—41%), and meat and poul-
try (3—70%), and the majority of positive samples
are isolated from seafood (31—72%) [3]. The iden-
tification of foodborne Aeromonas spp. shows a
predominance of A. hydrophila [4—10].
Parker and Shaw [11] observed that aeromonads
possess virulence factors such as hemolysins,
aerolysins, proteases, adhesins, enterotoxins,
phospholipase and lipase. Infections caused by
aeromonads can lead to gastroenteritis, sep-
ticemia, meningitis, respiratory and hemolytic
uremic syndrome. According to some authors
[12—15], A. hydrophila affects humans and causes
gastroenteritis. Saavedra et al. [16] stated that
A. hydrophila causes hemorrhagic septicemia in
stressed fish or those suffering from other illnesses,
thereby posing health risks to consumers.
The use of antibiotics is one of the most
important factors influencing the emergence of
resistance in bacterial pathogens. Multi-resistant
A. hydrophila were isolated from different parts
of the world and are reported to be resis-
tant to penicillin and ampicillin, but sensitive
to aminoglycosides, tetracycline, chlorampheni-
col, trimethoprim-sulfamethoxazole, quinolones,
[1,17]. However, the increase in A. hydrophila
resistance to antibiotics is a public health con-
cern; therefore, there should be a continuous and
concerted effort to monitor the existence of this
opportunistic pathogen globally [18].
Despite the vast information on the isolation and
characterization of A. hydrophila from seafood, lit-
tle information exists on the antibiotic resistance of
A. hydrophila from meat, meat products and dairy
products. The objective of this report is to review
the prevalence of antibiotic-resistant A. hydrophila
in different food sources.
Antimicrobial resistance of A.
hydrophila in different foods
Seafood
Over the last five decades, there has been an
increased production of fish at the global scale.
The marketing of fish as a food increased by an
average annual rate of 3.2%, which exceeds the
annual growth of the global population (1.6%). The
global per capita consumption of fish increased
from 9.9 kg in 1960 to 19.2 kg in 2012. This impres-
sive growth is simultaneously due to population
growth, increasing income and urbanization, as
well as the extensive development of fish farming
and more efficient distribution channels [19].
Intensive fish farming is accompanied by a
number of bacterial diseases, resulting in the
increased use of antimicrobial drugs. The pre-
vention and treatment of fish diseases through
extensive application of antimicrobial agents con-
tributes to the development of antibiotic-resistant
bacterial strains [20]. Among these diseases, A.
hydrophila-induced septicemia is a serious disease,
which is treated with different antibiotics [21]. The
frequent use of antibacterial drugs in aquaculture
could lead to increased antimicrobial resistance
and unacceptable levels of drug residues in aqua-
culture products and the environment [22].
Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources
Daood [21] affirms that the development
of antimicrobial resistance in aquatic microbial
pathogens will significantly decrease the thera-
peutic efficiency of drugs. Furthermore, increased
antibiotic resistance confers additional virulence
properties to bacterial pathogens. Resistant A.
hydrophila strains isolated from seafood intended
for human consumption reported from different
parts of the world are summarized in Table 1.
Meat and meat products
The contamination of meat with Aeromonas spp. is
attributed to the washing of carcasses with water
containing Aeromonas spp. and poor hygiene during
processing and meat cutting and grinding [36]. Enci-
nas et al. [37] acknowledged the poor control of raw
meat and fat materials as well as inadequate san-
itary measures during processing as the cause for
contamination of meat products with Aeromonas
spp. According to Rajakumar et al. [38], chopping
boards in households are the reason for cross con-
tamination of meat with microbial pathogens of
animal origin. Handfield et al. [39], Singh [40], Enci-
nas et al. [37], Sharma Kumar [9] and Osman et al.
[10] asserted that A. hydrophila was the predomi-
nant species among Aeromonas spp. isolated from
meat and meat products and that some strains had
virulence factors. Similarly, A. hydrophila strains
isolated from meat and meat products are resistant
to a broad range of antimicrobial drugs as shown in
Table 2.
Milk and dairy products
The microbial contamination of raw milk depends
on the health status of the animals, the hygiene
of the housing and milking environments, and the
methods of cleaning and disinfecting the milking
machines [42]. Milk is an excellent medium for the
growth of microorganisms, including A. hydrophila,
due to its high moisture content, almost neutral
pH and nutrients. Pathogenic A. hydrophila, which
can cause gastroenteritis, could be transmitted
with milk [43]. The occurrence of A. hydrophila
is reported in raw milk [4,43,44], pasteurized
milk [4] and cheese [44—46]. The results show
that A. hydrophila is a contaminant of raw milk,
and the presence of the pathogen in pasteurized
milk and cheese is an indication of poor pro-
duction hygiene [47]. Some studies reported the
resistance of A. hydrophila to antimicrobial drugs
(Table 3).
537
Vegetables
The surface of vegetables can be contaminated
with different microorganisms depending on the
microbial population of their original environment,
their state, method of processing, storage time and
conditions [48]. The lack of adequate hygiene of
processed vegetables may contribute to the spread
of Aeromonas spp. In addition, raw, insufficiently
or minimum heat-processed food may be a source
of aeromonads causing foodborne intoxication in
humans [49]. The susceptibility of vegetable A.
hydrophila isolates is poorly studied. There are sev-
eral reports of [50,51] the resistance of Aeromonas
spp. isolates from foods, including vegetables, but
without differentiation of the types of foods. How-
ever, Palu et al. [49], Oladipo and Adejumobi [52]
and Adebayo et al. [48] confirmed the presence
of A. hydrophila in vegetables and provided data
about the resistance of isolates to antimicrobial
drugs (Table 4).
Antimicrobial resistance mechanisms of
A. hydrophila
According to Alcaide et al. [53], the resistance
of Aeromonas spp. to antimicrobial drugs has
increased because emerging resistance was demon-
strated not only in clinical isolates, but also
in aeromonads from food and water. Saavedra
et al. [16] demonstrate that the extensive use
of antimicrobial drugs for prophylaxis and treat-
ment purposes in humans and fish unquestionably
plays a role in the increased number of resis-
tant A. hydrophila strains. As reported by Adebayo
et al. [48], the spread of resistance to antimicro-
bial drugs in foodborne pathogens has increased
during the last decades, likely as a result of the
use of these drugs in livestock raised for human
consumption. The presence of resistance genes in
mobile elements, such as plasmids, transposons
and integrons, facilitates their rapid spread among
bacteria. These mobile elements, according to
Romero et al. [54], could be transmitted among
bacteria via three pathways, including lateral DNA
transfer, namely transformation, transduction and
conjugation.
The microbial resistance in aeromonads is
chromosomally mediated; however, ␤-lactamases
may be coded by plasmids or integrons [55].
Aeromonas spp. produce different ␤-lactamases,
which confer resistance to a broad spectrum of ␤-
lactam antibiotics. Chen et al. [56] describe four
groups of chromosomally mediated ␤-lactamases as
 538
Table 1 Antimicrobial resistance of A. hydrophila isolated from seafood.
Antibacterial agent Percentage of resistant strains
Carps Indian Tilapia Fish (not Prawn Channel Trouts Shrimps, Mussels
carp, Rohu, specified) Catfish Crabs,
Grass carp Cuttlefish
Amikacin 0 100
Amoxicillin 52.7 88; 100 100
Ampicillin 100 100 100 100 80 65; 100
Bacitracin 100 99; 100 100 80
Carbenicillin 100 82 100
Cefotaxime 0 12 9
Ceftazidime 27.7 0
Cefuroxime 0 25
Cephalothin 57 100 65 100
Cefoxitin 30.8
Chloramphenicol 0; 6; 28.2 5.5 0 0; 4.4 0 0 100 0
Ciprofloxacin 0 0 0 0 0 0 0
Clindamycin 100 25 100
Cloxacillin 100
Doxycycline 0 25 0
Erythromycin 52 50 0; 97.3 84.6; 98 0 43; 100
Florfenicol 0.5; 6
Flumequine 0; 37
Furaltadone 0
Gentamicin 0; 7.3 0 0; 8.2; 16.6 3; 3.9 0; 25 100
Imipenem 50 19; 100 0
Kanamycin 28.2 0 0; 89.9 96; 100 9
Linkomycin 0 100
Methicillin 100 90.3; 100
Nalidixic acid 0 1.8 0 12.5; 16.7 10.9; 17 9
Neomycin 0 94.4 80.9; 98 0 14 0

D. Stratev, O.A. Odeyemi

Nitrofurantoin 0 100 9
Norfloxacin 0 50
Novobiocin 94.5 98.8; 100 93; 100 100 100
Ofloxacin 12.5 0
Olaquindox 18
Oxacillin 100 62.5
Oxolinic acid 0 9
Oxytetracycline 41; 43; 56.5 40 4 43 0
Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources 539

follows: (1) Class A — broad spectrum ␤-lactamases;

[35]
100

0
100
64
0

36
27
(2) Class B — metallo-␤-lactamases; (3) Class C
— cephalosporinases; and (4) Class D — penicil-
linases. Class A ␤-lactamases confer resistance
to all penicillins, cephalosporins and monobac-

[34]
0

0
tams, but not cephamycins and carbapenems, and
are inactivated by ␤-lactamase inhibitors. This ␤-
lactamase class may also be plasmid-mediated.
Class B metallo-␤-lactamases are activated only

[16,32,33]
by penems and carbapenems, but not penicillins
24; 87.5

and cephalosporins. Class C cephalosporinases can

87.5

87.5

100
hydrolyze many ␤-lactams, such as cephamycins
75
29

0
and second- and third-generation cephalosporins,
and are resistant to ␤-lactam inhibitors such as
clavulanic acid, tazobactam, and sulbactam. Class
[31] D ␤-lactamases hydrolyze penicillins. Depending
0
4

on the produced ␤-lactamases, Fosse et al. [57]

classified 417 Aeromonas strains into 5 pheno-
types. The study demonstrates that A. hydrophila
89.9; 100
86.2; 98

41.9; 41

62.4; 80

80.9; 94
3.9; 5.8

produces ␤-lactamases from classes B—D; A. caviae

[17,30]

produces ␤-lactamases from classes C and D; A.

veronii produces ␤-lactamases from classes В and
D; A. schubertii produces ␤-lactamases from class
D; and A. trota produces ␤-lactamases from class
C. According to Walsh et al. [58], Aeromonas spp.
9.3; 13.8; 25

are not only capable of producing ␤-lactamases,

53.3; 100

[7,17,29]
50; 64.9
0; 99.6

0; 83.2

but also of expressing these enzymes in a coor-

95.8

dinated manner, indicating that the expression of

100

genes encoding ␤-lactamases is controlled by a sin-

gle mechanism.
Plasmids are extra-chromosomal DNA coding vir-
[28]

ulence determinants [59]. A. hydrophila carries

100
0
100
100
100
0

50

stable plasmids playing an important role in micro-

bial resistance and virulence. There is evidence for
the significance of these plasmids in the resistance
41.8

of A. hydrophila to antimicrobial drugs. After the

[27]
0

removal of a 21-kb plasmid, A. hydrophila became

sensitive to antimicrobial drugs to which it was
previously resistant. Castillo et al. [60] showed
that plasmids are mobile genetic elements carry-
[23—26]

ing microbial resistance genes and that they are

33.4
100

transmitted among bacteria of various species via

15
23
0

horizontal gene transfer. Plasmids transfer these

genes in the bacterial chromosome or may gather
together multiple genes conferring resistance. This
Trimethoprim-sulfamethoxazole

results in the emergence of additional bacterial

strains resistant to several antimicrobial drugs at
a time, i.e., multi resistance.
Class 1 integrons are most commonly detected
in resistant bacteria. They are transmitted hori-
zontally among bacteria of the same or different
Trimethoprim
Streptomycin

species and play an important role in confer-

Tetracycline
Polymyxin-B

Vancomycin
Tobramycin
Piperacillin

Rifampicin
Pefloxacin

Reference

ring resistance in Gram-negative bacteria. Lukkana

Penicillin

et al. [61] investigated the carriership of classes

1—3 integrons in 50 A. hydrophila strains found in
tilapia. Class 1 integrons were detected in 23 (46%)
540 D. Stratev, O.A. Odeyemi

Table 2 Antimicrobial resistance of A. hydrophila isolated from meat and meat products.
Antimicrobial agent Percentage of resistant strains

Lamb Chicken Fillet Meat, minced meat, sausage

Amoxicillin 100 100
Ampicillin 100 100 100 100
Bacitracin 100 100 100
Cefadroxil 100
Chloramphenicol 10 0; 11.6 0
Ciprofloxacin 0 0 0
Clindamycin 0
Cloxacillin 100
Erythromycin 65 62.8; 100 0 100
Gentamicin 5 0; 4.7 0
Kanamycin 90 0; 88.4 0
Nalidixic acid 10 16.3 0 0
Neomycin 95 0; 81.4
Novobiocin 90 93 100
Oxacillin 100
Penicillin 100 100
Polymyxin B 90 90.7
Rifampicin 0
Streptomycin 10 11.6 0
Sulfamethoxazole 5 11.6
Tetracycline 25 0; 23.2 100
Tobramycin 0
Trimethoprim 0
Trimethoprim-sulfamethoxazole 100
Vancomycin 80 83.7 0
Reference [38] [4,38,41] [29] [4,42]

A. hydrophila strains, whereas class 2 and 3 inte-
grons were not detected.
Aeromonas strains are sensitive to quinolones,
although rarely, resistance to these drugs is
reported. Quinolone-resistant A. hydrophila due to
chromosomal mutations in the gyrA and parC genes
encoding target enzymes (DNA gyrase and topoiso-
merase IV) were reported by Alcaide at al. [53].
The resistance to quinolones, according to Cattoir
et al. [62] and Sanchez-Cespedes et al. [63], may be
associated with plasmid-mediated proteins. QnrS
determinants were detected in Aeromonas strains.
Fish are treated with antibiotics through feed,
via injection or, sometimes, by placement in an
antibiotic solution. The non-consumed feed and
antibiotic-containing feces arrive at the sediment
at the basin bottom. There, the antibiotic residues
exert a selective pressure altering the sediment
microflora and select for antibiotic-resistant bacte-
ria. The determinants of antibiotic resistance,
emergence and selection in the aquatic environ-
ment can be transmitted through the horizontal
gene transfer of microbial pathogens [64].
In general, A. hydrophila is resistant to ␤-
lactam antibiotics. The resistance to these drugs is
chromosomally mediated, but is sometimes caused
by plasmids or integrons. The frequent use of
antibiotics for the treatment of Aeromonas infec-
tions results in increased levels of antimicrobial
drug resistance. This requires periodic monitoring
for selecting the proper therapeutic.
Public health significance of
antibiotic-resistant A. hydrophila
Microbial resistance is of crucial significance to
public health. The newly emerging strains and the
potential for transfer of multi resistance to other
bacteria has broadened the spectrum of microbial
pathogens that do not respond to treatment with
the usual antimicrobial drugs. The increased multi
resistance in bacteria is due to the uncontrolled
use of antimicrobial drugs in animals and medical
practice [60]. Notably, the amount of antibiotics
used in aquaculture practice is almost equal to that
used for the therapy of human diseases. As a result,
increased resistance is observed, which reflects the
efficacy of treatment for humans and fish [20].
Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources 541

Table 3 Antimicrobial resistance of A. hydrophila isolated from milk and milk products.
Antibacterial agent Percentage of resistant strains

Milk Coalho cheese Colonial cheese Kareish cheese

Amoxicillin 100 40 100
Ampicillin 100 40 100
Bacitracin 94.4
Cefadroxil 100 100
Cefazoline 88.8
Cefepime 5.9
Ceftazidime 35.3
Ceftriaxone 17.6
Cefalotin 5.9
Chloramphenicol 22.2 0
Ciprofloxacin 0 29.4
Cloxacillin 100 100
Erythromycin 55.5; 100 36 100
Gentamicin 16.6 1 5.9
Kanamycin 77.7
Methicillin 94.4
Nalidixic acid 0; 88.8 0
Neomycin 55.5
Novobiocin 83.3
Penicillin 100 40 100
Polymyxin B 16.6
Rifampicin 94.4
Tetracycline 83.3 17
Trimethoprim 27.7
Trimethoprim-sulfamethoxazole 100 14 100
Vancomycin 94.4
Reference [4,42,43] [45] [46] [42]

Table 4 Antimicrobial resistance of A. hydrophila isolated from vegetables.

Source Antimicrobial resistance (%) Reference
Salads Augmentin, Ceftriaxone, Nitrofurantoin, Gentamicin, Cotrimoxa- [48]
zole, Amoxicillin, Ciprofloxacin, Streptomycin (100%), Ofloxacin,
Tetracycline, Erythromycin, Chloramphenicol (0%)
Lettuce Ampicillin (88.5%), Tetracycline (7.7%), cefotaxime, ceftazidime, [49]
imipenem, amikacin, gentamicin, tobramycin, ciprofloxacin, sul-
famethoxazole/trimethoprim and chloramphenicol (0%)
Beans Amoxicillin, Streptomycin, Chloramphenicol, Erythromycin, Nitro- [52]
furantoin, Tetracycline (100%), Gentamicin, Ofloxacin, Augmentin,
Ciprofloxacin, Cotrimoxazole, Ampiclox, Cefroxine (0%)

According to Goni-Urriza et al. [65], rivers Conclusion

receive wastewater that may contain antimicrobial
drugs and resistant commensal bacteria normally
inhabiting the aquatic environment, such as A.
hydrophila. These microorganisms may become a
reservoir of genes encoding resistance to antimi-
crobial drugs, as suggested by Rhodes et al. [20].
The researchers demonstrated the spread of tetra-
cycline resistance plasmids between A. hydrophila
and E. coli as well as between men and aquaculture
in different geographical regions.
It is important to continuously monitor antibiotic-
resistant A. hydrophila in different foods across
the global. Additionally, there must be a database
for this purpose to access information. Although
an expert meeting of the FAO, OIE and WHO [66]
in Geneva concluded that antimicrobial residues
in foods pose lower risks to human health than
the presence of bacteria resistant to antimicrobial
drugs, the presence of such bacteria in foods is a
542
potential threat for human health because resis-
tance may be spread among bacteria, impeding the
treatment of illnesses.
Funding
No funding sources.
Competing interests
None declared.
Ethical approval
Not required.
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