Rev. sci. tech. Off. int. Epiz.

, 2013, 32 (2), 497-507

Bacterial infections from aquatic species:

potential for and prevention of contact zoonoses
O.L.M. Haenen (1)*, J.J. Evans (2) & F. Berthe (3)
(1) Central Veterinary Institute of Wageningen UR, Laboratory for Fish, Shellfish, and Crustacean Diseases,
P.O. Box 65, 8200 AB, the Netherlands
(2) United States Department of Agriculture, Agricultural Research Service, Stoneville, MS, 38776, United
States of America
(3) European Food Safety Authority, Animal Health and Welfare Panel, Largo N. Palli 5/A, Parma, I-43100, Italy
*Corresponding author: Olga.Haenen@wur.nl

Summary
As aquaculture production and the consumption of aquaculture products increase,
the possibility of contracting zoonotic infections from either handling or ingesting
these products also increases. The principal pathogens acquired topically from
fish or shellfish through spine/pincer puncture or open wounds are Aeromonas
hydrophila, Edwardsiella tarda, Mycobacterium marinum, Streptococcus iniae,
Vibrio vulnificus and V. damsela. These pathogens, which are all indigenous to the
aquatic environment, have also been associated with disease outbreaks in food
fish. Outbreaks are often related to management factors, such as the quality and
quantity of nutrients in the water and high stocking density, which can increase
bacterial loads on the external surface of the fish. As a result, diseased fish are
more likely to transmit infection to humans. This review provides an account
of human cases of zoonoses throughout the world from the principal zoonotic
pathogens of fish and shellfish.
Keywords
Aquaculture Bacteria Fish Prevention Zoonosis.

Introduction
Zoonosis refers to a disease that can be transferred from
animals, whether wild or domesticated, to humans. With
the global growth of aquaculture and the increasing volume
of international trade in live aquatic animals and their
products (37), zoonoses require special attention. The
increasing interface between humans and aquatic animals
which may harbour infectious agents is a potential public
health concern. Despite an increased awareness of zoonotic
disease agents, their diagnosis in humans by clinicians
and medical practitioners is often hampered by a poor
knowledge of the zoonotic potential of disease agents in
aquatic species and the associated clinical signs (34).
Potential biological contamination of aquaculture products
can occur from bacteria, viruses, parasites and biotoxins
(46, 85). The location of the farm, the species being
farmed, water temperature, husbandry systems, postharvest processing, and habits in food preparation and

consumption are among the main factors influencing the

risk associated with aquatic animals and their products.
Zoonotic infections can be divided into:
a) topically acquired infections, caused by contact with
aquatic animals or their products
b) foodborne infections, caused by the ingestion of raw or
undercooked aquatic products.
Pathogens may be indigenous to the aquatic environment
or occur as the result of environmental contamination, due
to, for example, farms being located in polluted areas, the
use of excreta as fertiliser and faecal effluents from human
sewage, animal farms or wild animals (Salmonella, Shigella,
pathogenic Escherichia coli, Yersinia, Brucella, Edwardsiella).
This paper presents an overview of the zoonotic potential of
topically acquired (contact) bacterial infections caused by
Vibrio vulnificus, Edwardsiella tarda, Streptococcus iniae and

498

Mycobacterium marinum from aquaculture species, and how

to prevent them.

Topically acquired (contact)

bacterial infections
The principal bacteria topically acquired by humans
from fish, shellfish or crustaceans, through spine/pincer
puncture or open wounds, are: V. vulnificus, M. marinum,
S. iniae, E. tarda (48), Aeromonas hydrophila (59) and, less
importantly, Erysipelothrix rhusiopathiae (13, 43). Although
most fish-associated wound infections are self-limiting,
more serious cases are associated with an underlying
immune deficiency or incompetence in the patient, highly
virulent strains, a large inoculum, deep penetration of the
skin, or a combination of these factors. Patients develop
mild-to-severe infections (7, 26, 82) which, as in the case of
V. vulnificus, may prove lethal (5, 12, 52).
Groups most at risk of topically acquiring zoonotic bacteria
from fish include aquaculture professionals; fish culturists,
processors, and handlers; and commercial and recreational
fishermen and fisherwomen. They routinely have direct
skin contact with fish, often in humid indoor facilities and
at temperatures close to the optimal growth conditions for
bacteria. Individuals who are immunocompromised, and
have open skin injuries and/or are pierced by fish spines,
are at risk of developing a zoonotic infection. In 2012,
Verner-Jeffreys et al. (83) found V. vulnificus, V. cholerae
and M. senegalense in Garra rufa fish, used as pedicure fish
for humans. It can be inferred that immunocompromised
visitors to wellness centres are at risk from this practice.
Data on the prevalence and incidence of topically acquired
zoonotic infections from fish are scarce, as many are not
reported or diagnosed. Apart from a few reviews (5, 25,
35, 59, 65), published reports often chronicle a single case.
In addition, cases of human infection with these bacteria
are not usually notifiable. Vibrio vulnificus infection in
humans is notifiable in the United States (USA), and is
currently being considered for possible notification in the
Netherlands (O.L.M. Haenen, personal communication).
A 2009 workshop held on zoonotic infections from fish
and shellfish (41) identified the need to analyse the current
literature and promote more systematic reviews of the
available evidence.
Vibrio vulnificus, V. parahaemolyticus, V. damsela (28) and
V. cholerae are the principal species of Vibrio involved in
human infections (5), but there are at least 12 different
species described which have zoonotic potential (1).
Non-pathogenic strains of these species also exist.
Most cases reported in Europe are the result of wound

Rev. sci. tech. Off. int. Epiz., 32 (2)

infections caused by seawater or seafood exposure, which

can become systemic and even lethal in susceptible,
immunocompromised people (31, 32, 44). Other zoonotic
bacterial agents include M. marinum, which causes fish
tank granuloma in workers handling infected fish (46).
It has been isolated from ornamental and food fish (27,
44, 79, 80), but there are no reports of illness associated
with the consumption of farmed finfish or crustaceans
(85). Erysipelothrix rhusiopathiae and S. iniae are considered
occupational hazards for people handling fish, affecting
mainly immunocompromised individuals. Edwardsiella
tarda causes gastroenteritis but can also cause generalised
topical infections in humans, either from contact with or
ingestion of fish which harbour the bacteria (35). Table I
provides an overview, from the literature on human cases,
of the four principal potential zoonotic bacteria topically
acquired from aquaculture animals.

The principal contact zoonotic

bacteria from fish
Vibrio vulnificus
Vibrio vulnificus is a microorganism that is frequently found
in warm coastal waters (14). It has been isolated from
seawater, sediments, plankton and shellfish (oysters, clams,
crabs) in the Gulf of Mexico and off the Atlantic and Pacific
coasts of the USA (75). The prevalence of pathogenic vibrios
in waters depends on environmental factors, such as water
temperature, salinity and phytoplankton concentration (32,
73). The presence of Vibrio spp. has also been reported in
Europe, where levels are generally low, except in bivalves
(9, 39, 64).
The species vulnificus has been subtyped into three biotypes,
with serovars: biotype 1 in crustaceans and humans (74),
biotype 2 in eels (10, 77), among others, and biotype 3
in tilapia (11). A polymerase chain reaction was developed
(69) to subtype biotype 2 into potential zoonotic strains
(serovar E). Biotyping is no longer considered accurate for
subtyping. Current subtyping is based on sequence data,
which showed that biotype 2 strains were polyphyletic
(70). Biotype 2 was thought to be a pathovar, i.e. one of a
set of strains of V. vulnificus with the pathogenic potential to
infect fish and cause vibriosis (70).
In aquaculture and in the wild, V. vulnificus is known to
cause disease and is a serious pathogen of Japanese eels (62)
and European eels (10, 30). Affected eels show extensive
haemorrhages and severe necrosis (24, 38). Clinical signs
include haemorrhaging on the body surface, and in the
gastrointestinal tract, gills, heart, liver and spleen (6). Since
1991, the bacterium has been isolated 23 times from indoor

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Rev. sci. tech. Off. int. Epiz., 32 (2)

Table I
Human cases of topically acquired zoonotic infections by the four principal bacteria
Bacteria
Vibrio vulnificus

Edwardsiella tarda
Streptococcus iniae

Mycobacterium marinum

Country or region
USA
USA
USA
USA
Europe
Taiwan
USA, Europe &
Australia
Canada
Hong Kong
Singapore
USA
Taiwan
Worldwide
Worldwide
USA
France
Spain
Israel
Taiwan

No. of cases

Year

Reference

45,000
300*
90*
>900*
?
28
13
Low

from 1979
19881995
2005
19882006
19922008
19851990
<2004
?

75
34
16
17
3, 12, 23, 26, 67, 82
22
78
59, 65

12
2
3
7
1
35
166
653
63
35
20
3

19951996
2003, 2006
2004, 2009
20002004
2007
19662003
20002005
19931996
19961998
19911998
19921999
20042005

84
58
53
36
72
57
76
34
4
15
79
76

USA: United States of America

*Foodborne and topically acquired infections have not been segregated

cultured eels with deep ulcers and high mortality in the

Netherlands (26, 42). Vibrio vulnificus is a zoonotic invasive
pathogen (5). In low numbers, it causes primary wound
infections when a skin injury comes into contact with
infected seawater, fish or shellfish (23, 51, 55, 66), which
may develop into fasciitis necroticans (26, 56, 68, 82) and
even full sepsis and death (12). Immunocompromised
patients (52) suffering from liver diseases are at risk
(26). Mortality after wound infections may reach 25%.
After sepsis, mortality may reach up to 55%, mostly within
48h of the first appearance of clinical signs (19). Most
human cases are from biotype 1; however, since 1993,
biotype 2 has also been reported as a cause of human
disease, with some severe cases of fasciitis necroticans
and sepsis in patients (Fig. 1) (3, 19, 26, 61, 66, 71, 82).
Biotype 3 is a rather new type which has caused wound
infections after slaughtering tilapia in Israel (11).

Streptococcus iniae

Edwardsiella tarda

Topically acquired S. iniae infections have been reported

from 26 patients in five countries: Canada (84), Hong Kong
(58), Singapore (53, 54), Taiwan (72) and the USA (36).
Most of the affected individuals were Asian (85%) and
ranged in age from 40 to 88 years. Clinical signs included
cellulitis, septicaemia, endocarditis, arthritis, meningitis,
osteomyelitis, fever and abdominal distension and
pneumonia. Fifty-eight percent of the patients were known
to have handled or been exposed to fresh fish. Underlying

Edwardsiella tarda produces the disease commonly known

as fish gangrene, emphysematous putrefactive disease of
catfish or red disease of eels and referred to as Edwardsiella
septicaemia (ES), a systemic disease. The reader is referred
to Evans et al. (35) for a review of all aspects of Edwardsiella
tarda in particular, the economic, environmental and
social importance of the disease in fish and humans.

Streptococcus iniae, a Gram-positive bacterium, is a zoonotic

pathogen in fresh water and marine fish, causing disease
outbreaks in aquatic species (2) and invasive disease in
humans (8). This pathogen causes significant economic
losses, particularly in the tilapia and hybrid striped bass
aquaculture industries in the USA, Japan, Israel, South
Africa, Australia, the Philippines, Taiwan, Bahrain and
other countries. Evans et al. (33) provide an overview of
the epidemiological aspects of S. iniae in warm-water
fish, including global distribution, fish host susceptibility,
clinical signs of disease, sample collection, transport and
storage for successful survival and isolation, identification
by conventional, automated and molecular diagnostic
techniques, antibiotic sensitivities, and vaccination and
environmental influences on disease susceptibility.

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Rev. sci. tech. Off. int. Epiz., 32 (2)

a) During necrotic fasciitis with a bear claw incision for surgical debridement

b) After plastic reconstruction

Fig. 1
Hand of an eel farmer with necrotic fasciitis caused by a Vibrio vulnificus outbreak at his eel farm
Source: Dijkstra et al. (26) (reproduced by kind permission of The Netherlands Journal of Medicine)

conditions included chronic rheumatic heart disease,

osteoarthritis, hypertrophic obstructive cardiomyopathy,
duodenal ulcer and gallstones, diabetes mellitus, hepatitis
C-related liver cirrhosis, alcoholism, hypertension,
hypothyroidism and partial mastectomy; they were reported
in 35% of those contracting S. iniae infections (34).

Mycobacterium marinum
Mycobacterium marinum is an acid-fast rod-shaped
bacterium that causes worldwide chronic and severe
disease in many fish species in fresh water and brackish
and marine waters (20, 34, 40, 60, 63, 81). At least
167 species from more than 40 families of fish are susceptible
to Mycobacterium species (47).
In fish, M. marinum causes chronic systemic disease, with
granulomas in multiple organs and tissues, loss of scales,
loss of appetite, discoloration, apathy, exophthalmus,

slimeless skin, ulcers and eroded fins, followed by death

(40). Mycobacterium marinum has an optimum growth
temperature of 30C, and does not grow well at 37C.
In humans, M. marinum causes granulomatous inflammation
and nodular or diffuse granulomas of the skin, subcutaneous
tissues and tendon sheaths of fingers and hands, and
is referred to as swimming pool granuloma, fish tank
granuloma, fish handlers fish fanciers disease, or fish TB
(Fig. 2) (21). Invasive septic arthritis and osteomyelitis may
occur in immunocompromised hosts (29, 45, 49, 50, 57,
59), causing chronic skin lesions, congestion of the whole
finger and hand, and tenosynovitis. Between 1993 and
1996, 653 cases were confirmed in the USA, of which 49%
were associated with aquarium exposure, 27% with injury
by aquarium fish, and 9% with injury during bathing in
seawater (34). In France, 63 cases were reported between
1996 and 1998, of which 84% were associated with fish tank
exposure (4). Lahey (57) searched MEDLINE as far back as

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Rev. sci. tech. Off. int. Epiz., 32 (2)

injured their hands through puncture by fish (tilapia,

catfish, barramundi) or by a knife, resulting in chronic hand
infections. Clinicians failed to diagnose the causative agent.
To reduce the risks of topically acquired infection, people
should avoid direct contact with potentially contaminated
fresh or salt water if they have open cuts, scrapes or sores
on their skin.

Fig. 2
Man with a tender nodule on the dorsum of his right hand
(swimmer granuloma) caused by Mycobacterium marinum
Source: Christopher et al. (21) (reproduced by kind permission of the
Dermatology Online Journal).

1966 and discovered 35 invasive cases, occurring in patients

at an average age of 43 years, who had been treated with
immune impairment systemic steroids or chemotherapy,
or had acquired immunodeficiency syndrome (AIDS).
Sixty percent of these patients had tenosynovitis, 17% had
septic arthritis and 37% had osteomyelitis, but it is unclear
whether these conditions were attributable to infection. The
source of infection was exposure to water or injury through
fish spines or sharp edges on shellfish. The time until
diagnosis for these cases was 17 months from the onset of
symptoms, and the average duration of antibiotic therapy
was 11.4 months, with surgery taking place in 69% of cases
(34, 57). (In general, the average time to clinical diagnosis
is 4.4 weeks.)
Misdiagnosis and delayed treatment of M. marinum infection
are common because of its diverse manifestations (18).
The Centers for Disease Control and Prevention (CDC) in
the USA included M. marinum on their list of Emerging
infectious diseases from 2008. Additional topically acquired
Mycobacterium spp. with zoonotic potential include:
M. chelonae, M. fortuitum, M. abscessus, M. interjectum,
M.scrofulaceum, M. szulgai, M. similae and M.triplex.

People with compromised immune systems should avoid

handling fish or cleaning fish tanks. They should wear heavy,
waterproof gloves when handling or processing fish, and
cleaning home aquariums or fish tanks. Everyone should
wash their hands thoroughly with soap and water after
contact with fish or processing fish. It is also important to
ensure the regular and adequate chlorination of swimming
pools and fish tanks to kill any bacteria that may be present
(34, 41).
Bisharat et al. (11) reported that, after human cases of
infection with V. vulnificus were reported in Israel in 1996
and 1997, related to exposure to tilapia and carp, a new
policy was implemented. This policy prevented the selling
of live fish and stated that fins, scales and intestines should
be removed before marketing, the product must be cooled
throughout processing, and people should be advised
to purchase fish only from stores affiliated with the Fish
Farmers Association. This reduced the number of human
cases considerably.

Vibrio vulnificus
Antibiotics are necessary to treat V. vulnificus infections.
Effective antibiotics include tetracycline, third-generation
cephalosporins (e.g. ceftazidime), and imipenem, from the
carbapenem class (these are typically restricted in use to
avoid widespread bacterial resistance). In cases of wound
infection, aggressive debridement is necessary to remove
the necrotic tissue (26, 75).

Edwardsiella tarda
Edwardsiella tarda occurs sporadically in aquaculture
animals and humans. Extra-intestinal infections caused by
puncture wounds are susceptible to gentamycin, amoxicillin,
trimethoprim-sulfamethoxazole,
cephalosporins
and
oxyquinolones (59). As with other fish-derived zoonotic
bacteria, culture at lower temperatures is required.

Prevention and treatment

Streptococcus iniae

Zoonotic infections originating in aquatic animals are

under-reported, making risk analysis difficult. Haenen et al.
(unpublished data, 2008) interviewed 18 fish farmers and
processors. These farmers and processors usually worked
without gloves, and did not know about zoonotic risks and
prevention/hygiene. Most of those interviewed regularly

The prevalence of S. iniae can be underestimated,

particularly in Asian populations. Constraints for diagnosis
include the fact that the pathogen is often not identified by
conventional microbiological identification systems. There
is little surveillance of streptococci isolated from wounds
and tissues, and clinicians often fail to discover the patients

502

history of fish exposure. Prevention consists of using

protective equipment when cleaning and processing raw
seafood, and ensuring good hygiene (34).

Mycobacterium marinum
There are many factors which can prevent the diagnosis of
M. marinum:
the link to fishery products is often not recognised or
found
the presentation of this disease in humans is insidious
and non-specific
there is generally a delay between the onset of symptoms
and medical consultation (an average of five months)
there is a delay in definitive diagnosis of, on average,
4.4 weeks
the bacterium grows poorly at 37C, so is often missed
in hospital laboratories
clinicians often fail to find or recognise a history of fish
exposure (34).
Cheung et al. (18) reported that misdiagnosis often leads
to the inappropriate use of antimicrobials, extension of
the infection from the skin to the tenosynovium, and a
poor prognosis. Clinicians should be aware of this type
of infection, especially in subjects at risk (fishermen
and aquarium hobbyists), and those with a history of
trauma coupled with exposure to water or marine life.
He advises a proactive diagnosis through histopathology
and microbiology, with prompt antibiotic treatment with
rifampicin, ethambutol and clarithromycin. Debridement is
indicated in patients with deep-seated infections.

General recommendations
The control of topically acquired infections from aquatic
animals requires much improvement in communication
and medical diagnostics. It is of paramount importance to
develop and distribute zoonosis fact sheets to fish culturists
and fish processors, veterinarians, doctors, hospitals and
Veterinary Services.

Rev. sci. tech. Off. int. Epiz., 32 (2)

In addition, we need to better educate diagnosticians on the

clinical signs of these diseases in both fish and humans, as
well as on their culture conditions, prevention, hygiene and
therapy. It would also be wise to require zoonotic bacteria to
be notifiable to the appropriate international bodies, such as
the World Health Organization and the World Organisation
for Animal Health.
Further research is needed into issues of antibiotic resistance,
disinfection studies and risk assessment for these infections.

Conclusions
Topically acquired zoonoses from fish are not numerous,
but individual cases may be severe.
Topically acquired zoonoses are vastly under-reported
worldwide. This is partly the result of not recognising that
fish can be the source of zoonotic infection, and partly
because zoonotic agents derived from fish are still nonnotifiable in most countries.
Most of the topically acquired zoonoses in aquaculture are
caused by V. vulnificus, M. marinum and S. iniae. There is a
considerable lack of knowledge of the zoonotic risks from
fish among those at risk, either through their occupation or
by having a compromised immune system, and also among
diagnosticians. Anamneses and culture methods have
not been adapted to identify aquatic zoonotic agents and
should include lower incubation temperatures. In all, more
international research and much-improved communication
are needed to prevent topically acquired zoonoses from fish.

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Rev. sci. tech. Off. int. Epiz., 32 (2)

Infections bactriennes dorigine aquatique:

risques dexposition zoonotique par contact et prvention
O.L.M. Haenen, J.J. Evans & F. Berthe
Rsum
Au fur et mesure que le secteur de laquaculture produit davantage et fournit un
nombre croissant de consommateurs, on assiste un risque accru dexposition
des infections zoonotiques lors de la manipulation ou de lingestion de ces
produits. Les principaux agents pathognes pouvant tre transmis lhomme
par contact direct de plaies cutanes avec des poissons ou des crustacs
infects, ou suite une coupure par des artes ou des pinces, sont Aeromonas
hydrophila, Edwardsiella tarda, Mycobacterium marinum, Streptococcus iniae,
Vibrio vulnificus et V. damsela. Ces agents propres au milieu aquatique ont
tous t retrouvs lors de foyers dinfections bactriennes survenus chez des
espces de poissons destines lalimentation humaine. Ces foyers ont souvent
t imputs des facteurs relevant de la gestion des levages, par exemple une
qualit ou quantit inappropries de substances nutritives dans leau ou une
densit trop leve des populations, facteurs susceptibles daccrotre la charge
bactrienne sur la surface externe des poissons. De ce fait, les poissons infects
sont davantage mme de transmettre linfection lhomme. Les auteurs font le
point sur la situation mondiale des infections humaines par les principaux agents
pathognes zoonotiques prsents chez les poissons et les crustacs.
Mots-cls
Aquaculture Bactrie Poisson Prvention Zoonose.

Infecciones bacterianas procedentes de especies acuticas:

probabilidad y prevencin de las zoonosis por contacto
O.L.M. Haenen, J.J. Evans & F. Berthe
Resumen
A medida que se intensifican la produccin acucola y el consumo de los productos
de la acuicultura, tambin aumenta la probabilidad de contraer infecciones
zoonticas al manipular o al ingerir esos alimentos. Los principales patgenos
que el hombre contrae por va tpica a partir de peces o crustceos, ya sea al
lesionarse con espinas o pinzas o a travs de una herida abierta, son Aeromonas
hydrophila, Edwardsiella tarda, Mycobacterium marinum, Streptococcus iniae,
Vibrio vulnificus y V. damsela. Todos estos patgenos propios del medio acutico
tambin han sido vinculados con brotes infecciosos en peces destinados al
consumo humano. A menudo los brotes guardan relacin con factores zootcnicos
como la calidad y cantidad de nutrientes presentes en el agua o una elevada
densidad de poblacin, que pueden elevar la carga bacteriana en la superficie

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Rev. sci. tech. Off. int. Epiz., 32 (2)

externa de los peces. Una consecuencia de ello es la mayor probabilidad de que

los peces enfermos transmitan la infeccin al ser humano. Los autores exponen
una serie de casos descritos en distintas partes del mundo de zoonosis humanas
causadas por los principales patgenos zoonticos de peces y crustceos.
Palabras clave
Acuicultura Bacterias Peces Prevencin Zoonosis.

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