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A N D E R S M A R IN E IN S T IT U T E
0 0 3 1 6 CiG 'ï
Bo-lqii ’”71
L e tte rs in A p p lie d M ic ro b io lo g y 2 0 0 0 , 31, 3 5 9 - 3 6 3
Incidence and identification of mesophilic Aeromonas spp.
from retail foods
K. N e y t s 1, G. H u y s2, M. U y tte n d a e le 1, J. S w in g s 2 a n d J. D e b e v e r e 1
la b o ra to r y o f Food M icrobiology a nd Food Preservation, a nd 2Laboratory of Microbiology, University of Ghent, Belgium
2 0 1 /0 0 : re c e iv e d 18 Ju ly 2 0 0 0 a n d a c c e p te d 2 0 Ju ly 2 0 0 0
K . N E Y T S , G . H U Y S , M. U Y T T E N D A E L E , J . S W I N G S A N D J . D E B E V E R E . 2 0 0 0 . S ix ty -eig h t food
sam ples w ere exam ined for th e presence o f m eso p h ilic Aeromonas species b o th qualitatively
and q u antitatively. A erom onads w ere isolated fro m 2 6 % o f th e vegetable sam ples, 7 0 % of
th e m e at and p o u ltry sam ples and 7 2 % o f th e fish and sh rim p s. N u m b e rs o f m otile
aerom onads p rese n t in th e food sam ples varied from < IO2 cfu g_1 to > 10s cfu g ~ '. G L C
analysis o f F A M E s was used to identify a selection o f p resu m p tiv e Aeromonas colonies to
fenospccies or genom ic species level. Aeromonas strain s belonging to th e Aer. caviae
com plex, w hich also includes th e potentially path o g en ic genospecies H G 4 , w ere m ostly
isolated from vegetables b u t w ere also found in m eat, p o u ltry an d fish. I n ad d itio n , three
strain s o f th e v iru len t taxon Aer. veronii biovar so b ria H G 8 w ere isolated from p o u ltry and
m in ced m eat. All m em bers o f th e Aer. hydrophila com plex, p red o m in an t in th e fish, m eat
and p o u ltry sam ples, w ere classified in th e n o n -v iru le n t taxon H G 3 . A lth o u g h the
significance o f Aeromonas in foods rem ains u n d efin ed , th e isolation o f Aeromonas H G 4 and
H G 8 strains from a variety o f retail foods m ay indicate th at these p ro d u c ts can act as
possible vehicles for th e dessim ination o f fo o d -b o rn e Aeromonas gastro en teritis.
IN TR O D U C TIO N
carefu lly m o n ito re d in fo o d stu ffs as a possible so u rc e o f
Aerom onas species are w idely d istrib u te d in th e aquatic
e n v iro n m e n t, in c lu d in g ra w and p rocessed d rin k in g w ater
(H o lm es et al. 1996), a n d have b e en fre q u e n tly isolated
fro m vario u s food p ro d u c ts su c h as fish and shellfish, raw
m ea t, vegetables a n d raw m ilk (P a lu m b o
1996). M otile
aero m o n ad s are c o n sid e re d as e m e rg in g fo o d -b o rn e p ath o ­
gens b ecause it w as showrn th a t som e Aerom onas food iso­
lates can p ro d u c e different, v iru le n c e facto rs, not only at
o p tim al g ro w th te m p e ra tu re , b u t also at refrig e ratio n tem ­
p e ra tu re s (M e rin o et al. 1995). T h is m ay be o f im p o rtan ce
for re frig e rated food p ro d u c ts th a t usually have an
e x te n d ed sh elf-life a t th is te m p e ra tu re . A lth o u g h th e exact
role o f th ese v iru le n c e fa cto rs in th e path o g en esis o f m otile
Aeromonas species is still n o t fully e lu c id ated , re p re se n ta ­
tives o f th ese tax a have b e en in c rim in a te d in cases o f
h u m a n g a stro en teritis, p a rtic u la rly in c h ild ren younger
th a n 2 years, th e e ld e rly a n d im m u n o c o m p ro m ise d patients
(Jo sep h 1996). F u r th e r , A erom onas species are freq u e n tly
associated w ith tra v e lle rs’ d ia rrh o e a (H ä n n in e n el al. 1995;
Y am ada el al. 1997). C o n se q u e n tly , aero m o n ad s sh o u ld be
fo o d -b o rn e infections.
P h e n o ty p ic c h ara cte ristics o f Aeromonas spp. h a v e been
u se d to d iffe re n tia te betw een en v iro n m en ta l stra in s and
th o se stra in s cau sin g g a stro en teritis. H isto rically , m otile
aero m o n ad s w ere p h e n o ty p ic ally classified in to th e species
A er. hydrophila, A er. sobria a n d A er. caviae, a c c o rd in g to
th e c rite ria o f P o p o ff (1984). W ith th e in tro d u c tio n o f
D N A - D N A h y b rid iz atio n tec h n iq u e s (P o p o ff el al. 1981),
th e tax o n o m y o f th e g en u s Aeromonas has b e co m e m u ch
m o re refined and c o n se q u en tly , th e use o f biochem ical
c h ara c te ristic s alone for th e reliable id en tificatio n o f
u n k n o w n Aerom onas isolates is no lo n g er adequate.
C u rre n tly , th e g en u s A erom onas co m p rises at least 14 geno­
m ic species o r D N A h y b rid iz atio n g ro u p s (H G ), o f w hich
som e have n o t y et b e en n a m e d (H u y s el al. 1996).
In te re stin g ly , m o st p a th o g e n ic Aeromonas stra in s group
p re d o m in a n tly in th re e o f th ese genom ic species, Aer.
hydrophila H G 1 , A er. caviae F IG 4 and Aer. veronii biovar
so b ria H G 8 (A ltw egg el al. 1990). As m o st su rv ey s used
m a in ly p h e n o ty p ic tec h n iq u es for th e identification o f
Aerom onas food isolates, few reliable data are available on
th e p re v alen c e o f th e se Aeromonas tax a in foods.
Correspontknce to: D r Kristien Neyts, Laboratory o f Food Microbiology and
Food Preservation, University o f Ghent, Coupure Links 653, 9000 Gent,
Belgium (e-mail: kristien.neyls@rug.ac.be).
© 2 0 0 0 T h e S o c ie ty for A pplied M icrobiology
T h e objectives o f th is stu d y w ere: (i) to d e te rm in e the
p re v alen c e o f Aerom onas spp. in a w ide variety o f retail
foods, b o th qualitativ ely (a b se n c e /p re se n c e p e r 25 g) and
360
K. N E Y T S E T A L .
q u a n tita tiv e ly (cfu g ~ ') a n d (ii) to a s s e s s th e taxonom ic
d iv ersity o f th e isolated stra in s to genom ic species (H G )
level u sin g g a s-liq u id c h ro m a to g ra p h ic analysis o f cellular
fatty acids.
FAME id en tificatio n of A ero m o nas is o la t e s
G a s -liq u id c h ro m a to g ra p h ic (G L C ) analysis o f cellular
fatty acid m eth y l e sters (F A M E s) W'as used to fu rth e r
d e te rm in e th e tax o n o m ic d iv ersity a m o n g 130 Aeromonas
isolates fro m fish (73), vegetables (41), and m ea t and p oultry(16). F A M E profiles w ere d e te rm in e d as described by
H u y s el al. (1995). E sse n tia lly , o v e rn ig h t c u ltu res w ere
M A T E R IA L S AND M E T H O D S
in o cu la te d on T r y p tic S oy A gar (15 g 1—1; D ifco ) a ccording
to th e q u a d ra n t streak m e th o d (M ID I, 1999). Cells w ere
S a m p l in g of fo o d s
A to tal o f 68 food sam ples, 27 v e g etab le sa m p le s, 23 p o u l­
try , re d m e a t and m eat p ro d u c t sa m p les, a n d 18 sam p les o f
fish a n d sh rim p s, w ere co llected fro m seven ran d o m ly
selected local retail sh o p s a n d su p e rm a rk e ts in F la n d ers,
B elg iu m . F o o d s w'ere p u rc h a se d in re g u la r co n su m er
h arv ested fro m th e th ird q u a d ra n t a fte r 24 h. F ollow ing
saponification o f th e cell lip id s, m éth y la tio n o f th e fatty
acids a n d e x tra c tio n o f F A M E s , th e w ash ed ex tra cts w ere
analysed by a G L C e q u ip p e d w ith a flam e io n izatio n detec­
packages a n d im m ed iately tra n s fe rre d to th e lab o ra to ry for
to r. T h e re su ltin g peak p a tte rn s w ere auto m atically id e n ti­
fied a n d c o m p a re d w ith th e p re d e te rm in e d lib rary profiles
o f a re p re se n ta tiv e d a ta b ase, A E R 4 8 C , w h ich con tain s the
analysis.
m ean F A M E profiles o f all c u rre n tly recognized D N A
h y b rid iz atio n g ro u p s (H G s) o r genom ic species w ith in the
genus Aeromonas.
Q u a n tita tiv e a n a l y s i s ( e n u m e r a t i o n of A erom onas
s p p .)
RESULTS
F o o d sa m p le s (30 g) w ere tra n s fe rre d aseptically to sterile
sto m a c h e r bags, d ilu te d 10-fold in p e p to n e saline solu tio n
[8-5 g N a C i r 1 (Vel), l g p e p to n e P 1 (O xoid), p H 7 0],
P r e v a l e n c e of A ero m o nas s p . in v e g e t a b l e s , poultry
a n d m e a t, fish a n d s h r i m p s
h o m o g en iz ed , a n d a 10-fold serial d ilu tio n p re p a re d . T w o
selective c u ltu re m edia w ere used for e n u m e ra tio n , nam ely
M e so p h ilic a ero m o n ad s w e re id en tified in 2 6 % o f th e vege­
table sa m p le s ex am in ed (T a b le 1). O n ly tw o sam ples (fen­
nel a n d g a rd e n sorrel) w ere p ositive by d ire c t plating
A D A p H 8-0 (A m p ic illin -D e x trin A gar) and m odified
B IB G p H 8-7 (m odified B ile S a lts -Irg a s a n -B rillia n t G re e n
(d e te ctio n lim it IO2 cfu g _1), in d ic a tin g aero m o n ad counts
o f betw een 2-9 x IO2 cfu g -1 and 4-9 x IO3 cfu g _1. A rela­
A gar) (N e y ts el al. 2000).
B o th m ed ia w ere in cu b a te d for 24 h a t 30 °C a n d p re ­
s u m p tiv e Aerom onas colonies e n u m e ra te d . Aeromonas
stra in s typically p ro d u c e yellow colonies o n A D A m ed iu m
tively h ig h p e rc e n ta g e o f p o sitiv e sam ples (7 0 % ) was found
for m eat a n d p o u ltry (« = 23) (T a b le 1). D e te c tio n o f m eso­
p hilic aero m o n ad s by d ire c t p la tin g w as o n ly p ositive for
a n d p u rp le colonies on m B IB G m e d iu m . T h r e e p re su m p ­
tive A eromonas colonies w ere su b c u ltu re d o n T ry p tic Soy
A gar (O x o id ) for 24 h, 30 °C , for p u rific atio n and subse­
q u e n tly id entified to genus level by ox id ase and catalase
testin g , G ra m
coloration a n d th e B B L
C rystal I D
kit
(B ecto n D ic k in so n C ockeysville, U S A ).
Q ua litativ e a n a l y s i s ( p r e s e n c e / a b s e n c e of A erom onas
s p p .)
F o o d sam p les (25 g) w ere tra n s fe rre d aseptically to sterile
sto m a c h e r bags, d ilu te d 10-fold in A lk alin e P e p to n e W ater
p H 8-7 (O xoid), hom o g en ized , a n d in c u b a te d for 24 h at 30
° C p rio r to inoculation o n to A D A a n d m B IB G m ed iu m .
P re su m p tiv e Aeromonas colonies w ere id entified as
d e sc rib e d above. F o o d sa m p le s w e re d efined as bein g posi­
tive for Aerom onas i f c o n firm ed A erom onas colonies w ere
iso late d o n e ith e r A D A o r m B IB G m ed ia.
five o f th ese sam p les (b aco n , c hicken b re ast m eat, h a m b u r­
ger, m in c e d m ea t 2 x ) . H o w ev e r, in one sam p le, aerom onad
c o u n ts exceeded 10s cfu g _1. T h irte e n (7 2 % ) sam ples o f
fish a n d sh rim p s ( « = 1 8 ) w ere c o n ta m in a te d w ith
A erom onas and in
10 o f th ese sam ples, th e aerom onad
p o p u latio n s ra n g e d fro m
(T ab le 1).
1-9 x IO2 to 2-4 x IO5 cfu g -1
In th e q u a litativ e analysis o f foods, no significantly d if­
fe re n t re su lts w ere o b ta in e d u sin g th e A D A o r m B IB G
m e d iu m (T a b le 1). S ign ifican tly m o re sam p les show ed a
h ig h level o f c o n ta m in a tio n u sin g th e A D A m ed iu m than
th e m B IB G m e d iu m for d ire c t p latin g o f food hom ogenates
(T ab le 1). I f ty p ical A erom onas w as p re se n t on b o th m edia,
e n u m e ra tio n w as a b o u t 0 -5 -1 '0 log u n it h ig h e r on the
A D A m e d iu m th a n on th e m B IB G m e d iu m . H ow ever, the
b ack g ro u n d flora w as significantly re d u ce d o n th e m B IB G
m ed iu m (0-5 -2 -0 log u n its for th e vegetable sam ples,
resu lts n o t sh o w n ). T h is in d icates th a t m B IB G is a m ore
selective m ed iu m . A ll p re su m e d Aeromonas colonies from
m B IB G m e d iu m w ere c o n firm ed as A erom onas sp., w hereas
© 2 0 0 0 T h e S o c ie ty for A pplied M icrobiology, L e tte rs in A p p lie d M ic ro b io lo g y , 3 1 , 3 5 9 - 3 6 3
A E R O M O N A S S P P . IN R E T A IL F O O D S
361
T a b l e 1 P re v a le n c e o f A erom onas s p p . in d iff e r e n t fo o d s
N o . s am p les w ith A erom onas s p p .
T o ta l
S o u rce
V e g e ta b le s
7 /2 7 (2 6 )* a
P o u ltr y a n d m e a t
1 6 /2 3 (7 0 )* b
p e r 25 g
> 100 g -1
ADA
m B IB G
ADA
m B IB G
6 /2 7
6 /2 7
2 /2 7
1 /2 7
P o u ltry
5 /6
4 /5
4 /5
1 /5
0 /5
R ed m eat
9 /1 4
8 /1 3
8 /1 4
1 /1 3
2 /1 4
M e a t p ro d u c ts
2 /3
2 /3
1 /3
1 /3
0 /3
F is h a n d s h rim p s
1 3 /1 8 (7 2 )* b
F is h
1 1 /1 4
9 /1 2
1 1 /1 4
9 /1 2
5 /1 4
S h r im p s
2 /4
0 /2
2 /4
0 /2
0 /4
3 6 /6 8 (53)*
2 9 /6 2 (4 7 )* k
3 2 /6 7 (4 8 )* k
1 4 /6 2 (2 3 )* x
8 /6 8 (1 2 )* y
T o ta l
« F ig u r e s in p a re n th e s e s in d ic a te p e r c e n t v alu es.
a’b—k—x’yD if f e r Cn t c h a ra c te rs in d ic a te sig n ific a n tly d iff e r e n t re s u lts ( P < 0 05 B in a ry L o g istic R e g r e s s io n , S P S S 9 0 fo r W in d o w s).
six ty p ical colonies picked from A D A w ere id en tified as
Pseudomonas sp. T h is in dicates th a t m B IB G b e tte r d iffer­
e n tia te s Aeromonas.
C ro ss -in o c u la tio n o f stra in s pick ed fro m e ith e r m e d ia on
th e o th e r m e d iu m revealed th a t b o th m e d ia are co m p le ­
m e n ta ry ; tw o o f 64 A erom onas isolates tak e n from m B IB G
d id n o t grow on A D A , and a n o th e r th re e o f th e 64 isolates
d id n o t p ro d u c e ty p ical Aerom onas colonies on A D A . O n
th e o th e r h a n d , 13 o f 99 isolates taken fro m A D A d id n o t
gro w o n m B IB G , a n d one o f th e 99 isolates did n o t p ro ­
d u c e ty p ical colonies o n m B IB G (resu lts n o t show n).
Iden tificatio n of A ero m o nas is o la t e s fro m v e g e t a b l e s ,
m e a t a n d p o u ltry , a n d fish
F ro m th e p re se n t su rv e y , 216 m eso p h ilic A erom onas isolates
w ere o b tain e d . F A M E w as used to fu rth e r d e te rm in e th e
ta x o n o m ic d iv ersity a m o n g 130 o f th ese isolates (73 isolates
fro m fish, 41 fro m vegetables a n d 16 fro m m eat a n d p o u l­
try ). T h e p re d o m in a n t h y b rid iz atio n g ro u p (H G ) o f m o tile
a e ro m o n a d s isolated fro m fish sam p les w as A er. hydrophila
H G 3 (5 9 % ), follow ed by re p re se n tativ es o f th e Aer. caviae
c o m p lex ( H G 4 a n d H G 5 A ) (1 2 % ). A sim ila r re su lt w as
o b ta in e d fo r th e m e a t a n d p o u ltry sa m p le s, i.e., 3 7 % o f th e
isolates w ere id en tifie d as A er. hydrophila H G 3 and 1 2 % as
b e lo n g in g to th e A er. caviae com plex ( H G 4 and H G 5 A ).
D IS C U S S IO N
In re c e n t years, th e n u m b e r o f re p o rts o n th e prev alen ce o f
A erom onas in food p ro d u c ts fro m vario u s geographical
re gions has in creased sig n ifican tly . F o r in stan c e, Ib ra h im
a n d M a c R ae (1991) r e p o rte d th a t A erom onas was p re se n t in
60, 58, 74 and 2 6 % o f in v estig a te d beef, lam b, p o rk and
m ilk sam ples, re sp ec tiv e ly , w hereas K rovacek el al. (1992)
fo u n d aero m o n ad s in 4 2 % o f th e food sam p les o rig in atin g
fro m a ran d o m se lec tio n o f re ta il o u tle ts in S w eden.
Aerom onas w ere also fo u n d in fish a n d fre s h salads (W alker
a n d B rooks 1993), fresh ly dre sse d lam b carcasses (S ierra
et al. 1995), oysters (T sa i a n d C h e n 1996), cheese a n d raw
cow ’s m ilk (M elas et al. 1999). In th e p re se n t stu d y , m eso­
p h ilic a erom onads w ere isolated fro m 2 6 % o f th e vegetable
sam ples, 7 0 % o f th e m e a t and p o u ltry sam ples a n d from
7 2 % o f th e fish a n d sh rim p s. B ecause o f th e obvious d iffer­
ences in sa m p lin g p e rio d , g eographical location, th e origin
o f th e sam ples and m eth o d o lo g y for analysis, it is difficult
to co m p are th e level o f A erom onas in cid en ce p u b lish e d by
d iffe re n t a u th o rs. H o w e v e r, th e p re se n t d ata clearly con­
firm th e w id esp read d is trib u tio n o f m o tile a ero m o n ad s in
retail foods, and also re v ea l a large v ariatio n in th e level o f
co n ta m in a tio n . N u m b e rs o f m o tile aero m o n ad s p re se n t in
th e food sam ples varied fro m
< IO2 cfu g -1 to > 10s cfu
In te re stin g ly , th re e stra in s (1 9 % ) isolated from m ea t a n d
p o u ltry co u ld b e assigned to H G 8 {Aer. veronii b iovar
sobria). In c o n tra st, isolates o b tain e d fro m vegetables w ere
g - 1 . T h e la tte r m ig h t b e a reflection o f p ro d u c t-sp ec ific
p ro p e rtie s th a t can significantly in flu en ce th e survival ra te
an d g ro w th c h ara cte ristics o f A erom onas, i.e., in itial con­
ta m in a tio n levels, ty p e o f p ro c essin g , m e th o d o f packaging
an d p re serv a tio n (P a lu m b o 1996).
d o m in a te d by stra in s belo n g in g to th e A er. caviae com plex
(7 1 % ) (H G 4 , FIG S A a n d H G 5 B ), follow ed by A er. hydro­
p h ila H G 3 (7 % ) a n d A er. bestiarum H G 2 (5 % ).
T h e b iochem ical classification o f Aerom onas isolates into
one o f th e th re e h isto ric a lly -d efin e d fenospecies, i.e., Aer.
hydrophila, A er. caviae a n d A er. sobria, is applied in the
© 2 0 0 0 T h e S o c ie ty for A pplied M icrobiology, L e tte rs in A p p lie d M ic ro b io lo g y , 3 1 , 3 5 9 - 3 6 3
16806
B lack w ell S c ie n c e
362
LAM
MS 828
24/10/00
RW
K. N E Y T S E T A L .
m ajo rity o f su rv e y s o f m o tile a ero m o n ad s in foods (H u d so n
et al. 1992; K ro v a c e k et al. 1992; G ra n u m et al. 1998). O n
th e o th e r h a n d , v ery few stu d ie s have re p o rte d identifica­
tion a t th e g e n o m ic species level. B ecause o f th e significant
lack o f d a ta for th e d iffe re n t taxa, ra p id m in ia tu rize d or
a u to m a te d sy ste m s u sin g a panel o f biochem ical tests are
in a p p ro p ria te fo r id en tific atio n o f m o tile a ero m o n ad s to
genom ic sp ecies level. As th e m ajority o f th e v iru le n t
A erom onas s tra in s b e lo n g to A er. hydrophila H G 1 , Aer.
caviae H G 4 , o r A er. veronii b io v ar so b ria H G 8 (A ltw egg
significance o f Aerom onas in foods re m a in s u n d e fin e d ,
alth o u g h th e re is a g ro w in g c o n ce rn a b o u t th e c o n su m p tio n
o f /ferow oK ös-contam inated food by y o u n g c h ild re n , the
eld erly a n d th e im m u n o c o m p rim is e d .
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M .,
S te ig e rw a lt,
A .G .,
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el al. 1990), a reliable identification o f food isolates is
n ecessary to e stab lish th e risk associated w ith th e ir p reva­
tio n o f A erom onas g e n o s p e c ie s iso la ted fro m h u m a n s . J o u r n a l o f
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F A M E s w as u se d to id en tify a selectio n o f p re su m p tiv e
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A erom onas colonies to fenospecies o r genom ic species level.
A erom onas stra in s b e lo n g in g to th e A er. caviae com plex,
w hich also in c lu d e s th e p o ten tially p ath o g en ic genospecies
H G 4 , w ere m o stly isolated from vegetables b u t w ere also
fo u n d in m e a t, p o u ltry a n d fish. In a d d itio n , th ree strain s
o f H G 8 w ere isolated fro m p o u ltry a n d m inced m eat. N o
te riz a tio n o f A erom onas h y d ro p h ila a n d A erom onas caviae iso lated
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H ä n n in e n , M .L ., S a lm i,
S .,
M a ttila , L ., T a ip a lin e n , R . and
re p re se n ta tiv e s o f H G 1 w ere fo u n d a m o n g th e selected
colonies as all m em b e rs o f th e A er. hydrophila com plex
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sible vehicles fo r th e d e ssim in a tio n o f fo o d -b o rn e
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tional d ata o n th e p ro d u c tio n o f v iru le n ce factors, su c h as
haem o ly sin s a n d cy to ly tic e n te ro to x in s, are re q u ire d to
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stra in s id en tifie d as A er. hydrophila sh o u ld be m o n ito re d in
th e ep id e m io lo g y o f A erom onas-zssociated h u m a n gastroen­
teritis, it is u n fo rtu n a te th a t th e identification m e th o d s
used in b o th stu d ie s d id n o t allow d isc rim in atio n am ong
H G 1 , H G 2 o r H G 3 o f th e A er. hydrophila com plex.
D e sp ite th e fact th a t p o ten tially p a th o g e n ic a erom onads
re s o lu tio n
g e n o ty p ic
a n a ly sis
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