Bacterial zoonoses of fishes: A review and appraisal of evidence for [626850]

Review
Bacterial zoonoses of fishes: A review and appraisal of evidence for
linkagesbetweenfishandhumaninfections
David T. Gauthier *
Department of Biological Sciences, Old Dominion University, Norfolk, Virginia 23529, USA
ARTICLE INFO
Article history:
Accepted22October2014
Keywords:
Bacteria
ZoonosisFish-borneEpidemiologyMolecularbiologyABSTRACT
Human contact with and consumption of fishes presents hazards from a range of bacterial zoonotic in-
fections. Whereas many bacterial pathogens have been presented as fish-borne zoonoses on the basisof epidemiologicalandphenotypicevidence,geneticidentitybetweenfishandhumanisolatesisnotfre-quentlyexaminedordoesnotprovidesupportfortransmissionbetweenthesehosts.Inordertoaccuratelyassess the zoonotic risk from exposure to fishes in the context of aquaculture, wild fisheries and orna-mentalaquaria,itisimportanttocriticallyexamineevidenceof linkagesbetweenbacteriainfectingfishesand humans. This article reviews bacteria typically presented as fish-borne zoonoses, and examines thecurrent strength of evidence for this classification. Of bacteria generally described as fish-borne zoono-ses, only Mycobacterium spp., Streptococcus iniae ,Clostridium botulinum , and Vibrio vulnificus appear to
be well-supported as zoonoses in the strict sense. Erysipelothrix rhusiopathiae , while transmissible from
fishes to humans, does not cause disease in fishes and is therefore excluded from the list. Some epide-miological and/or molecular linkages have been made between other bacteria infecting both fishes andhumans, but more work is needed to elucidate routes of transmission and the identity of these patho-gens in their respective hosts at the genomic level.
©2014ElsevierLtd.Allrightsreserved.
Introduction
Bacterial zoonoses of fishes have received increasing attention
asnewbacterialpathogenshavebeenidentifiedandimprovedmi-crobiological and molecular methods have enabled identificationof fishpathogensinhumanhosts.Thesezoonoticagentshavebeenreviewed previously (
Ghittino, 1972; Shotts, 1987; Nemetz and
Shotts,1993;LehaneandRawlin,2000;Boylan,2011;Haenenetal.,2013
).Ratherthanfocusingongroundcoveredbythispreviousbody
of work, the present article will examine what is known about thenature of zoonotic associations between bacterial pathogens ofhumans and fishes, and the evidence for their connections.
The term ‘zoonosis’ is generally defined as an infection trans-
missible from animals to humans. The World Health Organizationmakes a further distinction that zoonosis in its strict sense shouldbe used to describe cases in which vertebrate animals are neces-saryformaintaininginfectionsinnature,andhumansareaccidentalhosts (
PAHO, 2001 ). This latter definition is contrasted with
‘infections-in-common’,inwhichpathogensareacquiredbyanimalsandhumansfromcommonenvironmentalsourcesornon-vertebrateorganisms. It is not uncommon for infections-in-common, includ-ing foodborne infections, to be classified as a form of zoonosis(
Haenenetal.,2013 ),butthistosomedegreeobscuresthebiologyand true epidemiological connections of an infectious association.
Many bacteria generally considered as fish zoonoses are faculta-tive pathogens with an environmental niche and often it is notpossible to differentiate between infections-in-common and strictzoonoses. The present review will detail what is known about thenature of infections with various bacterial agents in humans andfishes, as well as their transmission routes.
When drawing linkages between human and fish infections it is
important to determine whether they are caused by the same or-ganism. Most of the existing literature is limited to phenotypic/biochemicaldescriptionsofisolatesfromfishesandhumans,andthereis a paucity of information as to whether infections in fishes andhumansarecausedbythesamestrains,serotypes,orinsomecases,species of bacteria. Use of molecular techniques has improved ourability to determine whether human infections have arisen directlyfrominfectedfishes,environmentalsources,orthroughexposuretotransiently colonized or contaminated fish products (
Table 1). Most
bacteria identified as piscine zoonoses by previous authors will becoveredinthisreview,withtheadditionof Lactococcus garvieae ,which
has not been discussed in previous reviews.
Gram positive bacteria
Clostridium botulinum
Clostridium botulinum is commensal in the intestines of marine
andfreshwaterfishspeciesworldwide,andcanalsobefoundinen-vironmental sediments and decaying organic matter. A potent
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E-mail address: dgauthie@odu.edu .
http://dx.doi.org/10.1016/j.tvjl.2014.10.028
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paralyticneurotoxinisproducedbythisbacterium,whichinduces
descendingparalysisinhuman( BeanandGriffin,1990 ).Oftheseven
recognizedbotulinumtoxintypes(A–G),typeEisinvolvedinmostcasesof humandiseaserelatedtofishconsumption,althoughtypesA and B are occasionally implicated (
Barrett et al., 1977 ). Disease
infishesdueto C. botulinum isuncommonandoccurswhenfishes
feed on decaying carcasses that have become anaerobic and thussupport growth of the bacterium. The disease is known as ‘bank-ruptcydisease’inearthenpondcultureof salmonids(
Roberts,2001 )
andhasalsobeendocumentedas‘visceraltoxicosis’of catfishesinsouth eastern USA (
Khoo et al., 2011 ). Human botulism has been
associatedwithconsumptionof contaminatedfishproducts,notablysmokedfishinArcticandnortherntemperateregions(
Hielmetal.,
1998;Faganetal.,2011 ).Pulsed-fieldgelelectrophoresis(PFGE)and
random amplified polymorphic DNA (RAPD) analysis reveal con-siderablegeneticdiversityamong C. botulinum (
Hielmetal.,1998 )
and PFGE has demonstrated links between food and C. botulinum
genotypes involved in individual outbreaks ( Leclair et al., 2006 ).
Erysipelothrix spp.
Erysipelothrix spp. include Erysipelothrix rhusiopathiae ,E.
tonsillarum (Takahashi et al., 1987 ) and E. inopinata (Verbarg et al.,
2004).Innon-humananimals,thediseasecausedby E. rhusiopathiae
is properly known as ‘erysipelas’, while in humans the disease isreferredtoas‘erysipeloid’;‘erysipelas’inhumansiscausedby Strep-
tococcus spp., primarily S. pyogenes and S. agalactiae . Human
infections with E. rhusiopathiae occur via contamination of cuta-
neous wounds and typically result in localized, painful, self-limitingcellulitis,withpurplediscolorationandoedema(‘fishrose’)(
ReboliandFarrar,1989;Wangetal.,2010 ).SystemicinfectionswithE. rhusiopathiae in humans are uncommon, but are often associ-
ated with endocarditis ( Reboli and Farrar, 1989 ). Among animals,
erysipelas is of greatest significance in pigs, in which it causes‘diamondskindisease.’ E. rhusiopathiae colonizesthemucouscoating
of fishes, apparently as a commensal, as it has not been reportedtocausedisease.Zoonotictransmissionof E. rhusiopathiae tohumans
occursamongfisheriesworkers(‘fish-handlersdisease’)(
Reboliand
Farrar,1989 ).Takahashietal.(2008) performedDNA–DNAhybrid-
izationon Erysipelothrix spp.fromvarioussources,mainlytoclassify
E. rhusiopathiae and E. tonsillarum ,ratherthantoexaminehostspeci-
ficity.Despitetheabsenceof geneticevidence,thelinkbetweenskinlesionsinhumansandhandlingoffishescolonizedby E. rhusiopathiae
supports the contention that this bacterium is a zoonotic agent.However,fishescouldalsoberegardedasamechanicalvector,sinceE. rhusiopathiae does not appear to cause disease in fish hosts.
Lactococcusgarvieae
Amongpreviouslydescribed‘groupDstreptococci’, Lactococcus
garvieae isthemostsignificantfishpathogenandhasrecentlybeen
described as a human pathogen, causing endocarditis, cholecysti-tis and diskospondylitis (
Chan et al., 2011; Kim et al., 2013 ).
L. garvieae was first isolated from cases of bovine mastitis, initially
asStreptococcus garvieae (Collins et al., 1983 ), and has been de-
scribedfromwarmwaterfishes,initiallyas Enterococcus seriolicida ,
whichwassubsequentlydemonstratedtobeajuniorsynonymforL. garvieae (
Teixeira et al., 1996 ).L. garvieae causes serious disease
in cultured warm water fishes, typically manifesting as acutehaemorrhagic septicaemia, with mortality and reduced growth(
Vendrell et al., 2006 ). Human infection with L. garvieae has been
associatedwithingestionofrawseafood( Chanetal.,2011;Kimetal.,
2013),seasonalpeaksin L. garvieae infectioninculturedfishes( Wang
etal.,2007 )andoccupationalfisheryexposure( Aubinetal.,2011 ).
Restriction fragment length polymorphism typing has demon-
strated considerable diversity among L. garvieae associated with
outbreaksof diseaseinfishesandlackof similaritybetweenpiscineandbovinestrains(
Eldaretal.,1999 ).UsingPFGE, Velaetal.(2000)
observedhighgenotypicdiversityamongisolatesfromfishes,cattle,humanbeingsandwater,withhighersimilaritiesamongstrainsfroma given host. There was no similarity between isolates from fishes,including amberjack ( Seriolaspp.) and ‘trout’, and a range of other
species(cattle,pigs,cats,dogsandhorses)byPFGE(
Kawanishietal.,
2006), nor between isolates from fish and dairy products by RAPD
or amplified fragment length polymorphism (AFLP) analysis(
Foschino et al., 2008 ). Comparative genomics of L. garvieae iso-
lates did not reveal clear linkages between strains from fishes andothersources(
Ferrarioetal.,2013 ),whereasseveraldifferences(e.g.
adhesingenes)potentiallycontributingtohostspecificityhavebeenidentified (
Miyauchi et al., 2012 ). The available genetic informa-
tionpointstowardsseparationof humanandfishstrains,andthereis limited epidemiological evidence to support transmission ofL. garvieae between fishes and humans. Therefore, the status of
L. garvieae as a fish-borne zoonosis is questionable.
Staphylococcus spp.
Staphylococcus spp.,specifically S. epidermidis and S. aureus ,ha v e
beenisolatedfromculturedfishesduringdiseaseoutbreaks(
Kusuda
et al., 1976; Baxa et al., 1985 ), but their pathogenic role is unclear
and these bacteria are not generally discussed as agents of fishdisease.
NemetzandShotts(1993) mentionapotentialhumanhealth
threat from Staphylococcus spp. due to enterotoxin synthesis in
spoiled food; however, to date there have been no reports of zoo-notic fish-borne infections with Staphylococcus spp.
Streptococcus spp.
Infection with Streptococcus spp. in fishes typically involves
Lancefield group B organisms ( Streptococcus agalactiae )o rTable 1
Summary of potential agents of fish-borne zoonosis.
Organism Type Transmission
routeEpidemiological
evidenceMolecular
evidence
Clostridium botulinum G+Ingestion ++
Erysipelothrix rhusiopathiae G+Inoculation +a−
Lactococcus garvieae
(Enterococcus seriolicida )G+Inoculation
Ingestion+−
Staphylococcus spp. G +NA −−
Streptococcus agalactiae G+NA − (+)b
Streptococcus iniae G+Inoculation ++
Mycobacterium spp. AF Inoculation ++
Nocardia spp. AF NA −−
Aeromonas spp. G −Inoculation
Ingestion+−
Edwardsiella tarda G−Inoculation
Ingestion+−
Other Enterobacteriaceae G−Ingestion +−
Francisella spp. G −NA −−
Leptospira spp. G −Ingestion +c−
Plesiomonas shigelloides G−Ingestion +−
Pseudomonas spp. G −NA −−
Vibrio damsela G−Inoculation
Ingestion+−
Vibrio vulnificus G−Inoculation
Ingestion++
Yersinia ruckeri G−NA ( +)d−
aE. rhusiopathiae is not known to cause disease in fishes, but is a commensal in
skin mucus.
bSingle report ( Evans et al., 2008 ).
cZoonotictransmissionviahostsotherthanfishesappearsmostlikelyinthisin-
stance.
dSingle report ( Farmer et al., 1985 ).
Strongevidenceorevidencefrommultiplesourcesisindicatedby‘ +’,weakorsingle
reference evidence is indicated by ‘( +)’ and no evidence (or evidence to the con-
trary)isindicatedby‘ −’.Epidemiologicalevidenceincludesidentificationof bacteria
by phenotypic/biochemical methods, whereas molecular evidence refers to dem-onstration of genetic identity/strong similarity between isolates from human andfish infections. Staining characteristics are given as Gram positive (G +) or negative
(G −), or acid-fast (AF).28 D.T. Gauthier/The Veterinary Journal 203 (2015) 27–35

Streptococcus iniae , which does not express Lancefield antigens. S.
agalactiae isanagentofmastitisincowsandneonatalsepsisinhumans.
InfectionwithgroupB Streptococcus spp.hasbeenreportedfromawide
variety of temperate and warm water fishes, presenting withhaemorrhagic septicaemia and, often, neurological signs (
Evans et al.,
2006).Evansetal.(2008) reportedgeneticsimilarityamonghumanneo-
natal,andpiscineanddolphin,isolatesof S. agalactiae fromJapanand
Kuwait,respectively.However, Pereiraetal.(2010) failedtofindgenetic
identity among S. agalactiae isolates from humans, fishes and cattle,
socurrentlythereislittlegeneticevidencetoimplicategroupBstrep-tococci as fish-borne zoonoses.
Streptococcus iniae , originally isolated from the Amazon river
dolphin, Inia geofrensis (
Pier and Madin, 1976 ), has been reported
in a variety of piscine hosts ( Evans et al., 2006 ).Weinstein et al.
(1997)identified zoonotic infection with S. iniaein a disease out-
break in Toronto, Canada, involving nine humans with cellulitisrelatedtohandlingrawfish(tilapiaorunknownspecies);onepatientalso had endocarditis, meningitis and arthritis. The PFGE patterndemonstrated an identical strain of S. iniaein all nine human pa-
tients, matching isolates from tilapia in local fish markets, as wellas from an outbreak of disease in tilapia in Virginia, USA, in 1993.TwoadditionalhumancaseswereidentifiedretrospectivelyinTexas,USA,in1991andOttawa,Canada,in1994(
Weinsteinetal.,1997 ).
Zoonotic infections with S. iniaehave been reported in Southeast
Asia,CanadaandHongKong,andareprimarilyassociatedwithpro-cessing and handling live fishes (
Lau et al., 2003; Koh et al., 2004 ).
Acid-fast bacteriaMycobacterium spp.
Mycobacteria are the best known zoonotic fish-borne bacterial
pathogens, causing granulomatous inflammation of the skin and,occasionally,deepertissuesinhumans,knownas‘fisherman’sfinger’,‘fish tank granuloma, ‘fish-fancier’s finger’ and other similarly de-scriptiveterms.Lesionsof thistypewerefirstdescribedby
Nordén
andLinell(1951) andattributedto‘ Mycobacterium balnei ’(now My-
cobacterium marinum )bySwiftandCohen(1962) .Diseasefromfish-
or water-borne mycobacterial infection in humans generally takestheformof superficialgranulomatousinflammation,usuallyof theextremities, but may involve deeper tissues, resulting in tenosy-novitis, bursitis, arthritis and osteomyelitis (
Lahey, 2003 ). Both
localizedand‘sporotrichoid’formsof thediseasearedescribed;theformerpresentswithnodularorulceratedlesions,whilethelatteris associated with lymphatic spread (
Lewis et al., 2003 ). The incu-
bation period in humans is variable, but can be protracted, takingweeks to months before symptoms are manifested (
Jernigan and
Farr, 2000 ).
Inrarecases,usuallyassociatedwithimmunocompromisedpa-
tients and/or corticosteroid therapy, disseminated infections mayarise,withcutaneous,pulmonaryorvisceralinvolvement(
Kingetal.,
1983;Hoetal.,2001;Streitetal.,2006 ).Thisisof particularconcern,
sinceaquaticmycobacterialinfectionsmaypresentsymptomsthatmimicarthritisorautoimmunedisorders,promptingtheuseof cor-ticosteroids(
Bartonetal.,1997 ).Disseminated M. marinum infection
hasalsobeenobservedinimmunocompetentindividuals( Vazquez
and Sobel, 1992 ). Fatalities, although rare, have been reported
(Tchornobay et al., 1992; Gould et al., 2004 ). Antibiotic therapy is
generallyeffectiveforaquaticmycobacterialinfectionsinhumans,although surgical excision of lesions may be required (
Lewis et al.,
2003; Petrini, 2006 ).
In addition to their direct effects, M. marinum and other non-
tuberculousmycobacteria(NTM)caninducecross-reactivitytoskintests based on purified protein derivative (PPD) of M. tuberculosis
and M. avium (
Jolly and Seabury, 1972; Lewis et al., 2003 ). Inter-
feron release assays have been developed to circumvent falsepositivity in PPD skin tests, but exposure to some NTM, includingM. marinum , may generate false positive results with these assays
(
Kobashi et al., 2009 ).
The thermal tolerance of Mycobacterium spp. is likely to be in-
volvedintheirlimitedabilitytoinfecthumansandspreadtodeepertissues.Growthof M. marinum isrestrictedtotemperaturesbelow
37°C,limitingmosthumaninfectionstothedistalextremities(
Kent
et al., 2006 ). This issue of temperature tolerance is also of rele-
vance to mycobacteria producing mycolactone toxin (MPM),including the human pathogen Mycobacterium ulcerans and the
closelyrelatedfishpathogen Mycobacterium pseudoshottsii (
Rhodes
etal.,2005 ).MostMPMdonotgrowat35°Candoftengrowpoorly
above 30°C ( Ranger et al., 2006 ), which likely limits transmission
tohumans.However,apparentzoonoticinfectionsduetoMPMhavebeen reported (
Chemlal et al., 2002; Williamson et al., 2014 ).
Mycobacteriosis affects a wide range of fish species worldwide
and most frequently manifests as chronic granulomatous inflam-mation in viscera and muscles, as well as ulcerative skin lesions(
Gauthier and Rhodes, 2009 ). Piscine mycobacteriosis, historically
associated with M. marinum ,Mycobacterium fortuitum and Myco-
bacterium chelonae , is also linked to infections with a wide variety
of othermycobacterialspecies,including Mycobacterium shottsii and
Mycobacterium pseudoshottsii (Rhodes et al., 2003, 2005 ), and My-
cobacterium salmoniphilum sp.nov.,nom.rev.( Whippsetal.,2007 ).
Mycobacteriosishasasignificantimpactonaquacultureandorna-mental aquaria; with the exception of limited reports of antibiotictreatment, the only treatment option is destruction of infectedanimals and decontamination of holding facilities.
Human infections with fish-pathogenic mycobacteria are gen-
erally contracted through exposure of wounds and skin abrasionsto contaminated water; the disease occurred relatively frequentlyin users of swimming pools before the widespread use of chlori-nation (
Petrini, 2006 ). Currently, most cases are associated with
exposure to aquaria ( Aubry et al., 2002 ), as well as injuries con-
tractedduringseafoodprocessingorpreparation( Clarketal.,1990;
Lawler, 1994 ).
There are substantial genetic differences between M. marinum
isolatesfromfishesandhumans( UckoandColorni,2005 ).Zebrafish
(Danio rerio ) develop acute disease when inoculated with human
isolatesof M. marinum ,butchronicinfectionwheninoculatedwith
fish isolates ( van der Sar et al., 2004 ). Fish isolates of M. marinum
are infectious for mice, producing footpad and deep tissue infec-tions(
Kentetal.,2006 ).Mycobacterialinterspersedrepetitiveunit
(MIRU) typing generally supports the separation of human andpiscine isolates of M. marinum , but this genetic structuring is not
absolute,withsomeoverlapbetweenhostgroupings(
Broutinetal.,
2012).Geneticlinkagesbetweenhumaninfectionswith M. marinum
and fish sources have been demonstrated using PFGE ( Tsai et al.,
2007; Slany et al., 2013 ) and AFLP ( Doedens et al., 2008 ); however
inonecase,itislikelythatexposurewastowaterborne M. marinum
inoculated via a fish spine injury ( Tsai et al., 2007 ).
A wide range of other NTM reported in humans has also been
reported from fishes, especially M. fortuitum ,M. chelonae , and My-
cobacterium abscessus (Piersimoni,2009;Kothavadeetal.,2013 ),but
also Mycobacterium peregrinum (Pagnoux et al., 1998 ),Mycobacte-
rium scrofulaceum (Ishiietal.,1997 )and Mycobacterium haemophilum
(van Coppenraet et al., 2007 ).Mycobacterium spp .are often pre-
sumptivelytracedbacktoaquariumoraquariumfishsourcesusingeither phenotypic species identification or identification based onhousekeepinggenes(
Pateetal.,2005;Beranetal.,2006;Slanyetal.,
2012). However, this level of resolution is insufficient to confirm
relationships between human and fish infections, given consider-able infra-species diversity among the mycobacteria and the highdegree of conservation among housekeeping genes. For example,mycobacteria in the M. marinum clade, which are >99% similar to
one another at the commonly sequenced 16S rRNA locus, includesuch phenotypically diverse species as the human pathogen M.29 D.T. Gauthier/The Veterinary Journal 203 (2015) 27–35

ulcerans,extremelyslow-growingfishpathogens M. shottsii and M.
pseudoshottsii , and the relatively rapidly growing generalist M.
marinum. Furthermore, the phenotypically distinct species Myco-
bacterium gastri and Mycobacterium kansasii are 100% identical at
this locus. Analysis of additional genes, such as hsp65 and rpoB,
allows differentiation of species in most cases, but caution is stillnecessaryinattributinghumaninfectionstofishsourcesbasedevenonmulti-locussequencetyping(MLST).Thisisexemplifiedbyastudyinwhich Mycobacterium szulgai wasisolatedfromahumanpatient,
and both aquarium water and fish in the patient’s home; PFGE re-vealed identity between water and human isolates, but the fishisolate was markedly different (
Abalain-Colloc et al., 2003 ).
Nocardia spp.
Infection with Nocardia spp. in humans is primarily attributed
toNocardia asteroides and the closely related species Nocardia
farcinica ,Nocardia brasiliensis and Nocardia otitidiscaviarum .Nocar-
diosis in humans manifests in a variety of ways, primarilypneumonia,cutaneousulcersandwoundinfections,andoccursmorefrequentlyinimmunocompromisedpatients(
LedermanandCrum,
2004). Nocardial infections are also observed in fishes, and are at-
tributed to N. asteroides (Roberts, 2001 )o r Nocardia seriolae
(previously Nocardia kampachi )(Kudo et al., 1988 ). To date, no in-
formationisavailableonepidemiologicalorgeneticlinkagesbetweenpiscine and human nocardiosis, and therefore evidence of zoono-sis is lacking.
Gram negative bacteriaAeromonas spp.
Aeromonas spp.occurinfreshwaterhabitatsworldwideandare
implicated in community-acquired and nosocomial infections ofhumans (
Janda and Abbott, 2010 ). Human infections demonstrate
seasonality, with most cases reported in spring and autumn, pos-sibly mirroring increased numbers of pathogenic Aeromonas spp.
inaquaticenvironments(
KhardoriandFainstein,1988 ).Aeromonas
spp. infections arising from wound exposure have been associ-ated with handling seafood, particularly opening shellfishes(shucking)(
FlynnandKnepp,1987 ).Aeromonas salmonicida isamajor
pathogen of fishes, causing furunculosis in salmonids and cyprin-ids, but this species is not reported to be a human pathogen.
Weiretal.(2012) cites Aeromonas spp.asthemostcommonzoo-
notic bacterium isolated from ornamental fishes; however, amongthesereports,onlyasinglecasestudyindicatedalinkagetohumandisease,andthiswasnotconfirmedbybiochemicalorgenetictesting(
CremonesiniandThomson,2008 ).Sukroongreungetal.(1983) ex-
amined isolates from outbreaks of disease due to Aeromonas spp.
in fishes and concomitant cases of diarrhoea in humans; most fishisolateswere Aeromonas sobria ,whereasmosthumanisolateswere
A. hydrophila , and there was little overlap in biochemical typing
between Aeromonas isolates of the same species originating from
the two hosts.
Edwardsiella spp.
The three species recognised in the genus Edwardsiella are
Edwardsiella ictaluri ,Edwardsiella tarda (synonym Edwardsiella
anguillimortifera )and Edwardsiella hoshinae .Afurtherfish-pathogenic
species, Edwardsiella piscicida , has been proposed (
Abayneh et al.,
2013).E. ictaluri is a serious pathogen of catfishes ( Ictalurus spp.),
causingentericsepticaemia( Hawkeetal.,1981 ),butisnotknown
toinfecthumans. E. hoshinae istypicallyisolatedfromreptilesand
birdsand,althoughithasbeenisolatedfromhumanfaeces,itsroleasananimalorhumanpathogenisquestionable(
Jandaetal.,1991 ).
Human infections with E. tarda are characterized primarily by
bacterial gastroenteritis, although wound infections and systemicconditions, such as septicaemia and meningitis, are also observed,as are extraintestinal infections (
Clarridge et al., 1980; Janda and
Abbott, 1993 ).E. tarda may be found in the faeces of asymptom-
aticpeople( JandaandAbbott,1993 ).Riskfactorsfordiseaseinclude
exposuretoaquaticenvironments,aswellastofishes,reptilesandamphibians. E. tardacauses haemorrhagic and necrotic disease in
marine and freshwater fishes, including Edwardsiella septicaemia
in a variety of species, and ‘red disease’ in eels (
Wakabayashi and
Egusa, 1973 ).
There are few reports linking E. tarda from fishes directly to
human infections. E. tardain a Belgian infant was identical in API
(bioMerieux) biotype and antibiotic susceptibility to isolates fromanangelfish( Pterophyllum scalare )inanaquariuminthesamehome
(
Vandepitteetal.,1983 ).Presumedinfectionoriginatingfromapet
turtlewasreportedby Nageletal.(1982) ,althoughcultureormo-
lecular data supporting the linkage was not provided. Molecularanalysisof humanandfishisolatesof E. tardagenerallyshowsclear
differences(
Nuccietal.,2002;Abaynehetal.,2012;Yangetal.,2013 ).
Genomicanalysishasindicatedthat E. tardagenotypegroupEdwGI
is most closely related to E. ictaluri and contains most fish patho-
genicstrains,whereasEdwGIIcontainshumanandalimitednumberof fish isolates (
Yang et al., 2012 ). Whole genome comparisons of
E. tarda from various sources have revealed a clear divergence
between fish and environmental isolates, but also horizontal genetransferofahumanenteropathogenicvirulencefactortoafishisolate(
Nakamura et al., 2013 ).
OtherEnterobacteriaceae
Enterobacteriaceae areubiquitouslydistributedinavarietyof en-
vironmentalnichesandanimalhosts,andavarietyof specieshavebeen isolated from fishes, including enteropathogenic Escherichia
coli(
Shotts,1987 )and Salmonella spp.(Minette,1986 ).Isolationgen-
erallyoccursfromintestinalcontentsormucous;therefore,itappearsthat, while fishes can transiently harbour a variety of enterobac-teria, true infections are not common. Outbreaks of salmonellosisassociated with aquaria have been reviewed by
Weir et al. (2012) .
In several instances, identical isolates have been recovered fromhumanandtankwatersources,althoughtheroleof fishesinmain-taining Salmonella spp. in contaminated aquaria is unclear.
Contamination of fishes and fish products with enterobacteria is awidespreadconcerninfoodhandlingandhygienepractices,andbothSalmonella spp. and E. colihave been linked to foodborne illness,
with freshwater fishes or fish products likely serving as a vehicle(
Piérard et al., 1999; Terajima et al., 1999; McCoy et al., 2011 ).
However, evidence for these bacteria as strict zoonoses is limitedand cases where human infections are linked to fish consumptiongenerally do not provide evidence that infections originated withthe fishes and not from another source during food handling.
Bacteremia due to Klebsiella pneumoniae has been reported in
conjunctionwithhandfishing(
Reaganetal.,1990 );however,plasmid
typingof theorganismisolatedfromtheblooddidnotindicatesim-ilarity with K. pneumoniae in the water where the infection was
presumablycontracted,and fishes werenotsampled in thisstudy.Infection with Serratia marcescens , a pathogen of humans (
Hejazi
andFalkiner,1997 ),hasbeenreportedinwhiteperch( Morone amer-
icana)(Baya et al., 1992 ) and a bonnethead shark ( Sphyrna tiburo )
(Camusetal.,2013 ).However,noassociationbetweenpiscineand
human infections with S. marcescens has been demonstrated.
Francisella spp.
Francisella tularensis causestularemiainhumansandtherelated
bacterium Francisella philomiragia comb. nov. (formerly Yersinia
philomiragia ) has been isolated from cases of human disease
(Hollis et al., 1989; Wenger et al., 1989 ). In view of the high simi-
larity in housekeeping genes, literature concerning the naming ofFrancisella spp.issomewhatconfusingandspecieswithstandingin
nomenclature are in flux (
Birkbeck et al., 2011 ). The current litera-30 D.T. Gauthier/The Veterinary Journal 203 (2015) 27–35

tureappearstohaveconvergedonnamingfish-pathogenic Francisella
spp.as Francisella noatunensis incoldwaterand Francisella noatunensis
orientalis (syn. Francisella asiatica ) in warm water species. Human
infectionswiththesespecieshavenotbeenreported,and F. tularensis
orotherhuman-infectingstrainslikewisehavenotbeenisolatedfromfishes.Since F. noatunensis doesnotsurviveabove30°C(
Hawkeand
Soto, 2013 ), the zoonotic potential of Francisella spp. fish patho-
gens is not supported at present.
Leptospira spp.
Fishes may be infected experimentally with Leptospira spp.
(MaestroneandBenjaminson,1962;Davisetal.,2009 ),butnatural
infections have not been reported. Leptospirosis has been associ-ated with occupations involving fish handling and, especially, fishfarming. However, it is probable that, rather than being a fish-borne zoonosis, human infections are attributable to exposure tourinefromrodentpestsonfishfarmsand/orexposuretocontami-nated water (
Gill et al., 1985; Douglas, 1995 ).
Plesiomonas shigelloides
Plesiomonas shigelloides has been isolated from a wide range of
terrestrialandmarinemammals,reptiles,amphibians,birds,fishesandshellfishes(
Jagger,2000 ).Thebacteriumappearstobeanormal
or transient part of the intestinal biota in fishes; however, septi-caemiahasbeenreported(
ShottsandTeska,1989 ).Intwooutbreaks
of diarrhoea in humans due to P. shigelloides in Japan, there was
limitedoverlapwithserovarscollectedfromenvironmentalsources.
Arai et al. (1980) isolated P. shigelloides from 10.2% of freshwater
fishes and some isolates were the same serovars as found in diar-rheic human by
Tsukamoto et al. (1978) . The same serovars were
alsofoundinlocaldogsandcats.Although P. shigelloides caninfect
(or colonize) fishes, evidence for it being a true fish-borne zoo-notic is tenuous. P. shigelloides is frequently isolated from aquaria,
and at least one case of human infection has been associated withexposure to aquarium water (
CDC, 1989 ).Hori et al. (1966) linked
P. shigelloides infectioninhumanswithconsumptionof saltedfish.
Raworundercookedshellfishhavebeenimplicatedindiarrhoeaas-sociatedwith P. shigelloides inhumans(
Holmbergetal.,1986;Jagger,
2000), although this may be confounded with concomitant inges-
tion of local water ( Kain and Kelly, 1989 ).
Pseudomonas spp.
Pseudomonas spp. are motile aerobic rod shaped bacteria that
are common inhabitants of soil and water worldwide. Pseudomo-
nas fluorescens isanagentof necroticandhaemorrhagicdiseasein
avarietyof freshwaterandmarinefishes( AustinandAllen-Austin,
1985)andisanuncommonagentofhumandisease( Gershmanetal.,
2008).Pseudomonas aeruginosa is a well-known agent of human
pneumonia, especially in conjunction with other conditions, suchascysticfibrosis,andhasbeenisolatedfromfishviscera(
Leungetal.,
1992).Zoonotictransmissionof theseagentsfromfishestohumans
has not been documented.
Vibrio spp.
Vibriospp. are widely distributed in marine and estuarine en-
vironments and are often referred to as the marine equivalent ofaeromonads. A variety of Vibriospp. cause serious disease in wild
and cultured fishes, including Vibrio anguillarum , the agent of ‘red
pest’ in eels (
Roberts, 2001 ),Vibrio ordalii , which causes septicae-
mia in Pacific salmonids ( Schiewe et al., 1981 ),Vibrio salmonicida ,
which causes cold water vibriosis in Atlantic salmon and otherfishes (
Egidius et al., 1986 ), and Vibrio viscosus and Vibrio wodanis ,the causative agents of ‘winter ulcer disease’ in Atlantic salmon
(Lunder et al., 2000 ).
Among Vibriospp.thatcausediseaseinhumans, Vibrio cholerae
isof paramountworldwidehealthsignificance,particularlystrainswhichproducecholeratoxin.Toxin-producingstrainslargelybelongto the O1 serogroup, but non-O1/O139 serogroup strains may alsoproducetoxinsanddisease.Non-O1/non-O139(
Faramaetal.,2008 )
and O1 ( Blake et al., 1980 ) strains of V. cholerae have been impli-
catedinhumandiseaseoutbreaksassociatedwithconsumptionofshellfish and V. cholerae has been reported in water used to house
or transport ornamental fishes (
Smith et al., 2012 ). However, V.
cholerae is rarely reported as a disease agent in fishes ( Reddacliff
et al., 1993 ) and its role as a fish-borne zoonotic is questionable.
The most common non-cholera human vibrioses are caused by
Vibrio vulnificus and Vibrio parahemolyticus .Theseinfectionsareas-
sociatedwithgastroenteritis,septicaemiaandwoundinfectionsinhumans, and are of particular concern because of their high casefatalityrate(3.6%)relativetootherentericbacteria(
Weisetal.,2011 ).
V. parahemolyticus causes food-borne illness associated with con-
sumption of shellfish ( Drake et al., 2007 ), but is reported rarely in
fishes(AustinandAustin,2007 ).RAPDprofilingof V. parahemolyticus
from fish in markets demonstrated overlap with isolates fromshellfishsources(
Yangetal.,2008 );thus,itisunclearwhetherthe
V. parahemolyticus were derived from fish products or from
cross-contamination.
Vibrio vulnificus causes disease in eels ( Tison et al., 1982 ) and
other fishes ( Li et al., 2006 ), and has been isolated from the intes-
tinal tract of bottom-feeding fishes ( DePaola et al., 1994 ). Three
biotypes of this species are described; biotype 1 is isolated mainlyfromwaterandhumans,andbiotype2isisolatedmainlyfromfishesand humans (
Amaro and Biosca, 1996 ). Specific polymorphic vari-
ants of the type IV pilus gene pilFare strongly associated with
resistance to human serum and thus potential for human infectiv-ityinallbiotypes(
Roigetal.,2010 ).Cohenetal.(2007) demonstrated
two major clades of V. vulnificus using MLST. Most biotype 1 clin-
ical isolates belonged to one clade and possessed a 33kb genomicislandthatmaybeassociatedwithhigherpathogenicityand/oren-vironmentalpersistence.Pathogenicityforfishesinbiotype2strainsisrelatedtothepresenceof a68–70kbvirulenceplasmid(
Roigand
Amaro,2009 ).Biotype2isfurtherseparatedintoserovarsA,Eand
I,whichareinfectiousforfishes,butof whichonlyserovarEappearsto have zoonotic potential (
Fouz et al., 2007 ). Biotype 3 has been
isolated from humans with septicaemia and wound infections inIsrael and has been postulated to be a hybrid between biotypes 1a n d2(
Bisharat et al., 1999, 2005 ), although this has been ques-
tioned by Cohen et al. (2007) .
V. vulnificus biotype2septicaemiahasbeenreportedinaperson
whohadhandledeels( Veenstraetal.,1992 ),andsequencingof vir-
ulencegenes( vvhAand vvp)demonstratedoverlapbetweenhuman
and eel biotype 2 isolates ( Wang et al., 2008 ). Human isolates of V.
vulnificus biotype2,serovarEcarryidenticalplasmidprofilestofish
strains,includingthe68–70kbvirulenceplasmid( RoigandAmaro,
2009). Linkages between fish and human clinical biotype 3 iso-
lates have also been demonstrated with variable number tandemrepeat(VNTR)analysis(
Brozaetal.,2009 ).MLSTtypingof fishiso-
latesinBangladeshiaquaculturedemonstratedclosesimilarity,butnot identity, of fish and clinical isolates (
Mahmud et al., 2010 ).
The current body of literature on genetic similarity between
humanandfishisolatesof V. vulnificus isbetterdevelopedthanmany
other presumptive bacterial zoonoses of fishes, and transmissionbetween fishes and humans appears to be supported, although itis apparent that infections may also be contracted from environ-mental sources.
Vibrio damsela (
Loveetal.,1981 ),now Photobacterium damselae
comb. nov. ( Smith et al., 1991 ), was first isolated from skin ulcers
indamselfish( Chromis punctipinnis )andhassincebeenisolatedfrom31 D.T. Gauthier/The Veterinary Journal 203 (2015) 27–35

other fishes, including turbot ( Scophthalmus maximus ), yellowtail
(Seriola quinqueradiata ) and sea bream ( Pagrus auriga )(Austin and
Austin, 2007 ). P. damselae infection in humans is primarily associ-
ated with skin wounds, leading to necrotizing fasciitis that can befatal (
Morris et al., 1982; Clarridge and Zighelboim-Daum, 1985;
Hundenborn et al., 2013 ). Two cases of V. damsela septicaemia in
humanshavebeenassociatedwithingestionof rawfish( Shinetal.,
1996; Kim et al., 2009 ). However, genotypes of human and fish
isolates have not been compared, and the degree to whichhuman V. damsela infections originate from fishes remains to be
determined.
Additional Vibriospp.,including Vibrio hollisae (Grimontia hollisae
comb.nov.;
Thompsonetal.,2003 ),Vibrio alginolyticus ,Vibrio fluvialis ,
Vibrio furnissii ,Vibrio harveyi (syn. Vibrio carchariae ),Vibrio
metschnikovii and Vibrio mimicus ,areassociatedwithdiseaseinfishes
and shellfishes, and are also occasionally isolated from cases ofhuman disease, particularly gastroenteritis and wound infections(
Austin,2010 ).However,directconnectionsbetweenfishandhuman
infections are tenuous and most cases appear to derive from con-taminationof woundswithseawater,spoilageof consumedfishandshellfish, or ingestion of raw shellfish.
Yersinia spp.
Severalmembersof thegenus Yersiniacausehumandisease,in-
cluding Yersinia enterocolitica ,Yersinia pseudotuberculosis and,most
notably, Yersinia pestis ,thecauseof bubonicplague. Yersinia ruckeri
causes enteric redmouth disease (ERM) of salmonids, which is as-sociatedwithsignificantaquaculturelossesworldwide(
Austinand
Allen-Austin, 1985; Tobback et al., 2007 ). A single human case of
infectionwith Y. ruckeri ,of uncertainclinicalsignificance,hasbeen
reported( Farmeretal.,1985 ).Severalother Yersiniaspp.havebeen
isolatedfrombothfishesandhumans,including Yersinia frederiksenii
and Yersinia intermedia (Sulakvelidze, 2000 ), but evidence of fish-
borne zoonotic infections in this group is lacking.
Conclusions
A variety of bacteria have been reported as potential fish-
bornezoonoticagents,butevidenceforzoonoticpotentialislimitedfor many of these organisms and few molecular genetic analysesof fish and human strains have been performed. The existing lit-eraturesupportsclassificationof C. botulinum ,S. iniae,Mycobacterium
spp.and Vibrio vulnificus asfish-bornezoonosesinthestrictsense,
i.e.thereissubstantialepidemiologicalandmolecularevidenceforlinkages between infections in both hosts. Epidemiological asso-ciations suggest zoonotic risks for other fish-associated bacteria;however, some do not cause disease in fishes (e.g. Erysipelothrix
rhusiopathiae ) and more work will be required to link human and
fish infections with other bacteria (e.g. Aeromonas spp., E. tarda,
L. garvieae ,P. shigelloides and V. damsela ). Other bacterial species
either lack significant evidence for epidemiological connectionsbetweenfishesandhumans,havemoreplausibletransmissionroutesnot involving fishes, or are most likely to be transmitted throughcontamination of food. Further molecular studies examining iso-lates from fishes and human disease outbreaks would be fruitfulindefiningepidemiologicalconnectionsandindeterminingthezoo-notic risk from bacterial fish pathogens.
Conflict of interest statement
None of the authors of this paper has a financial or personal
relationship with other people or organisations that could inap-propriately influence or bias the content of the paper.References
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