htematianal Journal

ofFoodMicn&&igy

International Journal of
Food Microbiology 27 (1995) 147-159

ELSEVI:ER

Improvement of Salmonella detection on motility

enrichment media by ferrioxamine E-supplementation
pre-enrichment culture
Peter Pless a, Rolf Reissbrodt

of

b,*

aFachabteilungfir das Veteriniirw~en beim Amt der Steiermirkischen Landesregierung,

Zimmerplatzgasse IS, 8011 Graz, Austria
b Robert Koch-lnstitut, Bereich Wemigerode, BurgstraJ?e37, D-38855 Wemigerode, Germany
Received 18 July 1994; accepted 18 November 1994

Abstract
Supplementation
of buffered
peptone
water with ferrioxamine
E in concentrations
ranging from 0.001 to 1.0 pg/ml significantly increased the motility of Salmonella on
MSRV and DIASSALM semi-solid enrichment media. Zone diameters of swarming S.
enteritidis and S. typhimurium increased more than twofold following use of pre-enrichment
cultures supplemented with 0.01 pg ferrioxamine E/ml. The activity of ferrioxamine E is
similar ;at 37C and 42C. Pre-enrichment of Salmonella in a variety of foods in supplemented buffered peptone water, with shaking at 37C for 6 h and motility enrichment at
42C for 16 h, enabled motile Salmonella to be detected in 1 day.
KeyworL;!s:Ferrioxamine

E-pre-enrichment;

Salmonella; Motility enrichment

1. Introduction

Rapjid detection of Salmonella in food by motility enrichment on Modified

Semisolid Rappaport-Vassiliadis (MSRV) media is widely recognised as an effective procedure for identifying contaminated products at low costs (De Smedt et al.,
1986; De Smedt and Bolderdijk, 1987,1989a,b; Van Netten et al., 1991; ODonoghue
and Winn, 1993; Pless et al., 1993; Van der Zee, 1994). Collaborative studies have
shown the method to be superior to conventional culture methods (Perales and
Audicana, 1989; De Smedt and Bolderdijk, 1990; De Zutter et al., 1991.) The

Corresponding

author. Tel.: 03943/679 2.58. Fax: 03943/679 207.

0168-160:5/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved

SSDI 0168-1605(94)00160-X

148

P. Pless, R. Reissbrodt /Int. J. Food Microbiology 27 (1995) 147-159

technique exploits the motility possessed by most SaImoneZZa strains. Semi-solid

media are unsatisfactory for detecting S. typhi and S. paratyphi A or other
non-motile strains. However, Holbrook et al. (1989) reported that the incidence of
non-motile strains of Salmonella is very low (approximately 0.15%). Successful
application of motility enrichment is dependent on the strength of motility as well
as the number of cells available (at least 60/m] neccessary according to De Smedt
and Bolderdijk, 1987) after pre-enrichment in appropriate media. Buffered peptone water supplemented with ferrioxamines E or G as selective growth factors
exhibited higher sensitivity and shortened incubation time of most Salmonella
serotypes isolated from the albumen of hens eggs (Reissbrodt and Rabsch, 1993).
Ferrioxamine E have been produced biotechnologically and acts in supplying
Salmonella with very well utilizable iron.
This paper reports on effectiveness of the combination of ferrioxamine E-supplemented buffered peptone water and of the modified semi-solid Rappaport-Vassiliadis media in isolation and identification of Salmonella.

2. Material and methods

Bacteria: Salmonella strains used in experiments detailed in Tables l-3 were
taken from the collection of the Nationales Referenzzentrum der Salmonellosen at
the Robert Koch-Institut, Bereich Wernigerode, Germany. Salmonella strains
listed in Tables 4 and 5 were from the collection of the Institut fiir Fleischhygiene,
Fleischtechnologie
und Lebensmittelkunde,
Veterinarrnedizinische
Universitat
Wien, Austria, and identified by the Gsterreichisches Bundesinstitut fur Bakteriologie und Serologie, Graz, Austria. Each strain was cultured overnight on
Nutrient agar (DIFCO, code no. 0001) incubated at 37C and its identity checked
serologically before use. The most probable number (MPN) technique was used to
determine the number of Salmonella cells inoculated. A plate-drop technique on
XLD-medium (Oxoid CM 469) using the spatula-method according to Baumgart
(1993) was used to determine the numbers of Salmonella for spiking the foods. The
S. enteritidis cells for spiking milk powder were sublethally injured by drying at
43C in condensed milk as described by Edel and Kampelmacher (1973).
2.1. Nutrient media

Buffered peptone water (BPW, Oxoid CM 509) and Modified semi-solid Rappaport-Vassiliadis medium (MSRV, Oxoid CM 910) were purchased from Unipath
Ltd., Basingstoke, England. Diagnostic semi-solid salmonella agar (DIASSALM
LAB 537) was kindly provided by LAB M, Topley House, Bury, England. The
media were processed as instructed by the manufacturers and novobiocin to
increase the selectivity added to MSRV and DIASSALM at a concentration of 20
mg/l. A modified Rappaport-Vassiliadis broth according to Pless et al. (1994) was
used in the impedance method. Ferrioxamine E, kindly provided by Dr. H.H.

P. Pless,R. Rekbrodt /Int. J. Food Microbiology27 (19%) 147-159

149

Table 1
Effectiveness of ferrioxamine E-supplementation of Buffered peptone water on swarming behaviour of
Salmonellastrains on DIASSALM and MSRV medium, incubated at 37C for 16 h
Ferrioxmine E
(kg/m)

0.000

O.cQl

0.010

0.100

1.000

2.000

DIASSALM

MSRV

S. enteritidis
327/94

S. typhimurium
104/94

diameter
(mm)

diameter
(mm)

56
50
50
48
54
70
60
70
68
62
70
73
60
69
68
45
30
37
42
36
60
65
60
62
63
50
45
40
50
40

Peters, Ciba-Geigy,
sterilization.

mean/
SD

51.60
3.29

66.00
4.69

68.00
4.85

38.00
5.79

62.00
2.12

45.00
5.00

28
35
40
36
32
45
33
40
42
37
40
35
45
42
38
35
22
24
30
24
45
35
37
41
37
35
25
17
21
29

Switzerland,

mean/
SD

34.20
4.49

39.40
4.62

40.00
3.81

27.00
5.39

39.00
4.00

25.40
6.99

was added

S. enteritidis
327/94

S. typhimurium
104/94

diameter
(mm)

diameter
(mm)

35
30
10
20
30
60
72
43
63
52
60
70
70
67
65
60
60
70
65
61
70
65
65
64
69
65
60
60
59
63

mean/
SD

25.00

10.00

58.00
11.02

66.40
4.16

63.20
4.32

66.60
2.70

61.40
2.51

to buffered

n.d.
25
25
27
29
35
32
43
39
34
30
35
30
34
30
35
27
35
34
30
33
35
38
39
31
25
32
20
24
27

peptone

mean/
SD

26.50
1.91

36.60
4.39

31.80
2.49

32.20
3.56

35.20
3.35

25.60
4.39

water

after

2.2. Evaluation of the effectiveness of ferrioxamine E-supplementation of BPW on the

swarming behaviour of Salmonella subcultured to MSRV and DIASSALM
Two to five cells of each of the Salmonella strains were added to 10 ml of fresh
blendecl albumen and stored at room temperature for 16-18 h. One part of each

P. Pless, R. Reissbrodt / Int. 1. Food Microbiology 27 (1995) 147-159

150

Table 2
Effectivness
of ferrioxamine
E-supplementation
of Buffered peptone
S. enteritidis 327/94 on DIASSALM
and MSRV medium, incubated
Ferrioxmine

diameter

0.000

50
45
45
45
50
45
75
90
85
85
90

0.010

behaviour

of

MSRV

DIASSALM

Gg/mi)

water on swarming
at 37C for 18 h

(mm)

diameter

mean/SD

mean/SD

(mm)

40
30
30
22
32
25
70
80
90
100
n.d.

46.67
2.58

85.00
6.12

29.83
6.21

85.00
12.91

mixture was then added to 10 parts of Buffered peptone water supplemented with
O-2 pg ferrioxamine E/ml and shaken for 6 h at 37C. 50 ~1 drops of each
enrichment culture were inoculated onto the surface of either MSRV or DIASSALM plates and incubated at 37C or 42 C for 16-18 h. The size of zones were
read from five plates of each of the trial groups.

Table 3
Effectiveness
of ferrioxamine
E-supplementation
of Buffered peptone water
S. enteritidis 327/94 and S. typhimurium 1@4/94 on MSRV-plates,
incubated
Ferrioxmine E
(p g/m1)

diameter

(mm)
o.ooo

0.010

1.000

42C

37C

3PC

S. enteritidis
327/94

31
35
30
32
33
62
62
60
60
61
60
55
56
57
58

on swarming behaviour of
at 37C and 42C for 18 h
42C

S. typhimurium
104/94
mean/
SD

32.20
1.92

61.00
1.00

57.20
1.92

diameter

(mm)
n.d.
20
17
19
16
28
34
34
34
n.d.
44
54
40
40
44

mean/
SD

18.00
1.83

32.50
3.00

44.40
5.73

diameter

(mm)
17
17
15
17
16
31
33
32
35
34
20
24
22
26
20

mean/
SD

16.40
0.89

33.00
1.58

22.40
2.61

diameter
(mm)
15
18
16
17
16
26
29
27
29
26
35
34
32
33
33

mean/
Sd

16.40
1.14

27.40
1.52

33.40
1.14

P. Pless, R. Reissbrod! /ht.

J. Food Microbiology 27 (1995) 147-159

151

2.3. Evaluation of the effect of ferrioxamine E-supplementation of BPW on the

swarming behaviour of Salmonella strains isolated on MSRVfrom artificially infected
food

Whole eggs, egg yolk and egg white were spiked with different amounts of
and origins (Table 3). The spiked samples
were mixed in a ratio of 1:lO with BPW without and with ferrioxamine E-supplementation (1.0 pg/ml) and incubated at 37C for 3, 5 and 8 h. After 3 and 5 h,
samples were taken and stored at 2C in a refrigerator. Three drops (ca. 0.1 ml) of
each of the pre-enrichment cultures were inoculated in separate spots on the
surface of MSRV plates. The MSRV plates were incubated at 42C for 21,lS or 15
h, respectively, and the zones of swarming estimated following the same method
for testing contaminated milk powder, chicken wings and potato chips (Table 4).
Additionally, the impedance changes in the BacTrac 4100 measuring system
(Bacteria Tracer, SY-Lab,3002 Purkersdorf-Vienna,
Austria) were measured according to Pless et al. (1994). 0.1 ml of the pre-enrichment culture after 3, 5 and 8
h were diluted with 9.9 ml of a modified Rappaport-Vassiliadis
broth and incubated at 40C for 22 h. Impedance output higher than 5% of the basic level in
hours was monitored as positive of Salmonella.
Salmonlella cells of various serotypes

2.4. Preliminary Salmonella test in the swarm zones

The C&esterase reaction was performed according to Olsson et al. (1991). 10 ~1
of MUCAP-reagent (4-Methylumbelliferylcaprylate,
kindly provided by Biolife,
Milano, Italy) were droped on the zone of swarming. A bright fluorescent spot on
MSRV and DIASSALM media exposed to 365 nm wavelength UV light for 3-5
min denoted the presence of migrating Salmonella.

3. Results
The swarming behaviour of Salmonella strains on MSRV and DIASSALM
plates was significantly improved after enrichment in Buffered peptone water,
supplemented with ferrioxamine E (Table 1). Few Salmonella cells, injured by
storage in albumen at room temperature overnight (2-5 cells/l0 ml albumen),
multiplied within 6 h to the number necessary for detection if inoculated directly
on the motility enrichment media.
Swarming zones of S. enteritidis 327/94 on MSRV plates were greater than
twofold1 larger when the Buffered peptone water pre-enrichment cultures were
supplemented with 0.001 to 1.0 pg/ml ferrioxamine E than zones formed following pre-enrichment in unsupplemented Buffered peptone water ( Tables 1 and 3).
Increasing amounts of ferrioxamine E up to 2 pg/ml BPW did not further
increase zone sizes. A similar effect was seen on DIASSALM plates (Table 1).
However, DIASSALM exhibited bigger swarming zones than MSRV even if

origin

egg

w3

serotype

S. enteritidis

S. enteritidis

Salmonella spp. used

250

25

600

60

200 ml
BPW

CdlS/

spiked
with

3
5
8
3
5
3
5
8
3
5

3
5
8
3b
5 *b
3
5
8
3
5

Time of
pre-enrichment (h)

from contaminated

22
22
22
32
32
32

1
32

1
33
30
22
32
32
33
22
33

ncg

neg
1

neg
1

033
133
133
2
2
2

032
2

133
3
032
033
233
233
3
233
3

22

33

32

##
##
##

##

##

##

##

011
311
332
333

010
211

333

0
322
333
333

220
322

33
22
33

33

32

32

ncg

33

##
##

##
##
##

##

with ferrioxamine E

011
122
232
011
1
2
233
3
3
232
333

233
233
233
2
3
3

032
222
2

without ferrioxamine E

without ferrioxamine E

with ferrioxamine E

egg yolk

whole egg

Diameter of swarm zone on MSRV-plates after pre-enrichment

Table 4
Influence of ferrioxamine E on the swarm zone size on MSRV of SaZmonella spp. pre-enriched

210
311

1
2
211
1
1
310

0
3
311
311

2
210

eggs

1
32

32
(1)
1

21

neg
neg

neg
neg

0
1

neg
neg

neg

220
333

300

1
2
0221
0
3
2
0221
0322

1333

2
2

3
##

0
2

0
2

0
0

0
0

with ferrioxamine E

0332
1333
2333
0
2
1333

0331
1333

without ferrioxamine E

egg white

2
\o

jj
h,
;
3
Y!
;;

%
g
2
B

8
c
B
i:

3
$
2
.9
?J
B
c;.

400

egg shell 40

avb*csee Table 5.

iiU??l

S. typhimu-

322
##

222
##

211
1

##

233
3

22
33
1

3
5

2
22

##
##

2
3

33
33

5
8

##
##

211
211

233
233

332
333

133
233

21
22

5
3
##
##

neg

211

33

332
##

133
2
032

1
3
1

8
3

1
2
0

*eiz

1
211
311
1

122
233
333
111

221

022

10

;;;;

3
##

3
1

0;;
;

2
0222
1
3
1

3
1

g
h

3
er
b
.J
3
%
E.
P
8
\

spp. used

serotype

S. enteritidIL%

S. enteritidis

Salmonella

food

Milk
powder

Chicken
wings

Unknown

Sublethally
injured

origin

70

700

70

spiked
with cells /
lOOmI

5
8
3
5

5
8=
3b
sgb
3
5
8
3
5
3
5
8
3
5

Time of
pre-enrichment (h)

Table 5
Influence of ferrioxamine
E on the swarming zone on MSRV
contaminated
milk nowder. chicken wines and nofafo chins

pre-enrichment

2
3

neg

neg
3
2
2
##
2
2
##
##
##
2
3

2
2

1
1
1
3

2
3

2
2

3
2
2

1
2

2
1
2
3

3
3

3
3
3
3
3

neg

2
1
2
3

3
3
0
3
3
##
##
3
3
##
##
##
3
##

with ferrioxamine E

2
1
0
2

2
3

15.5
15.0

n.d.

20.1
13.6
5.6

n.d.
15.7
10.6

n.d.
11.6

n.d.

without ferrioxamine E

following

without ferrioxamine E

3
3
0
3
2

output

Output of impedance
pre-enrichment
(h)

spp. and of the impedance

Diameter of swarm zone after

pre-enrichment

of Salmonella

15.5
15.2

n.d.

16.5
9.8
4.0

n.d.
11.8
7.1

17.6
11.0

n.d.

with ferrioxamine E

after

culture

from

Y
2
;8
*
P
;
%
\o

s.rubis
law

Potato
chips

Pepper

Naturally
contaminated

700

3
3
2
3

5
8
3
5
2
2

2
2
3
3

2
2

2
1
1
3

2
3

3
3
3

1
3

3
2
3
##

n.d.

14.2
12.2
-

n.d.

2 (1
n.d.
corn.) d
20
7.3
corn.) d
1
2(1
corn.) d

2
2
2

7.0

20.4

n.d.

14.5
11.9

18.2

indicated.
indicated additionally
a time of storage at - 2C of the same inoculated pre-enrichment
at 2C, respectively,
noted by * .
0 = one drop did not swarm; 1 = swarm zone up to 1 cm; 2 = swarm zone l-2 cm;

2
2
3
3

8
3
5

a Directly droped onto MSRV-plates

after the pre-enrichment
time
b Directly droped onto MSRV-plates
after the pre-enrichment
time
until the working day was finished. This means 3 or 5 h of storage
Diameter of swarm zone: neg = all three drops did not swarm;
3 = swarm zone 2-3 cm; ## = overswarmed
the whole MSRV-plate.
4 corn. = competitors,
non-Salmonella.
n.d. = not detected (non output > 5%) after 22 h.

tidis

S. enteri-

Chicken
wings

156

P. Pless, R. Reissbrodt /ht.

J. Food Microbiology 27 (199.5) 147-159

ferrioxamine E was not present. For S. enteritidis 327/94, supplementation of the

Buffered peptone water pre-enrichment culture with 0.01 pg/ml ferrioxamine E
enabled zone sizes on MSRV to develop to a size similar to those on DIASSALM
(Table 2). A decrease in zone size diameters occurred at ferrioxamine E concentrations of 0.1 pg/ml and 2.0 pgg/ml. Diameters of swarming zones differed dependent from preparation of the plates and of incubation time. However, ferrioxamine
E promoted the swarm behaviour of Salmonella as demonstrated in all the
experiments.
S. fyphimurium 104/94 showed smaller improvements of swarming behaviour
but also exhibited significantly larger swarm zones when supplemented with
ferrioxamine E.
The diameter of swarm zones is dependent on the incubation temperature of
the motility enrichment media (Table 3). The swarming zones of S, enteritidis
327/94 were significantly smaller in size when incubated at 42C compared to 37C
and behaved similarly to those of S. typhimurium 104/94. However, the swarming
behaviour of both the strains tested was promoted by ferrioxamine E-supplementation of BPW, at both 37C and 42C zones on MSRV were twice as large as those
resulting from unsupplemented BPW.
Whole egg, egg yolk and egg white were contaminated with different cell counts
of two S. enteritidk strains and one S. typhimurium strain, isolated from eggs.
Detection of swarming zones and their diameters on MSRV were significantly
improved by supplementation of Buffered peptone water with 1 pg/ml ferrioxamine E. Swarm zones could be seen after 3 or 5 h incubation in ferrioxamine
E-supplemented BPW seeded with 25-60 cells per 200 ml (Table 4). Contrarily, no
swarm zones were detected on MSRV inoculated with cultures of egg white in
BPW not containing ferrioxamine E after 3 h. The diameters of swarm zones in all
experiments conducted were enlarged by use of ferrioxamine E-supplemented
BPW. This principle was retained when more cells were inoculated and when
incubation time was increased to 8 h. Storage of the culture samples at 2C for 3 or
5 h did not significantly influence the swarming behaviour of the Salmonella strains
tested. Formation of swarm zones on MSRV and increase in their diameter
effected by ferrioxamine E-supplementation was most noticeable for egg white and
whole eggs. Larger zones were produced by egg yolk and ferrioxamine E-supplementation did cause any increase in diameter.
Similar results were obtained from contaminated milk powder, chicken wings,
and potato chips, respectively (Table 5). Low numbers (ca. 7 cells/ml) of sublethally injured S. enter-Z&s cells in milk powder after 5 h pre-enrichment in BPW
with ferrioxamine E produced swarm zones on MSRV of 2-3 cm. Using higher cell
counts no significant differences could be detected of pre-enrichment with and
without ferrioxamine E. Impedance changes denoting cell multiplication could be
detected significantly earlier after cultivation in ferrioxamine E-supplemented
BPW (Table 5). Swarming behaviour and impedance changes were the same when
pre-enriching without and with ferrioxamine E from chicken wings and potato
chips as they were for isolates from milk powder.

P. Pless, R. Rehsbrodt /ht.

J. Food Microbiology 27 (1995) 147-159

157

4. Discussion
The composition of motility enrichment media for Salmonella as well as the
temperature of incubation (at 42C, most of the competitors like E. cloaca or C.
&versus cannot swarm), pH of the medium and addition of iron and sulphite salts
were intensively studied and resulted in the present formulas of MSRV (Oxoid) or
DIASSALM (Lab M). For one-day detection of Salmonella by motility enrichment
a very effective pre-enrichment medium is needed. The use of M-broth described
by Sperber and Deibel (1969) has been reviewed by De Smedt and Bolderdijk
(1989b). Ferrioxamine E-supplementation of Buffered peptone water functions in
shortening the incubation time and increasing the sensitivity of pre-enrichment
culture of injured Salmonella [(Reissbrodt and Rabsch (1993)l. This supplementation is also very effective in improving the swarming behaviour of Salmonella
strains on MSRV and DIASSALM semi-solid motility enrichment media (Table 1).
As little as l-10 ng ferrioxamine E/ml BPW is necessary to increase the diameter
of swarming zones on MSRV greater than twofold in contrast to Salmonella cells
grown in BPW without supplementation.
The diameters of swarm zones on
DIASSALM are larger than those on MSRV ( Tables 1 and 2) after inoculation of
pre-enrichments that are not supplemented with ferrioxamine E. Pre-enrichment
of Salmonella enteritidis 327/94 in ferrioxamine E-supplemented BPW compensated for this advantage (Table 2). The effectiveness of ferrioxamine E-supplementation is detectable when incubating MSRV media at either 37C or 42C (Table
3).
Improved swarming of Salmonella on motility enrichment media was detected
over the range 0.001 to 1,0 pg ferrioxamine E/ml BPW. Addition of ferrioxamine
E to the motility enrichment media as well as 30 min incubation of the diluted cells
before inoculation applicated onto the surface of MSRV or DIASSALM plates
had no effect (data not shown). No effect was seen also after supplementation of
the modified Rappaport-Vassiliadis broth for impedance measurements.
It is assumed that repair of the injured cells and availability of a portion of
viable cells amongst the high number produced during pre-enrichment
are the
reasons of this effect. Investigations into the influence of ferrioxamine E on the
flagella-apparatus are in progress.
Ferrioxamine E is not able to feed E. coli or the Proteus-frouidenciaMorganella-group. This confers a selective advantage on Salmonella in motility
enrichment. The efficacy of pre-enrichment culture in BPW supplemented with
ferrioxamine E for recovery of different numbers of various Salmonella spp.
contai.ned in a variety of artificially contaminated foods is shown in Tables 4 and 5.
Salmonella could be detected on MSRV after enrichment for 3 h in 200 ml of
ferrioxamine E-supplemeted BPW. Detection of Salmonella by motility enrichment seems to be not influenced by storage the pre-enrichment samples at 2C for
5 or 3 h. The period of enrichment required for detection is dependent on the
number of Salmonella present in the food. The diameters of swarming zones were
larger than those from unsupplemented BPW.
Impedance changes were detected earlier by BacTrac 4100 when samples were
enriched in ferrioxamine E-supplemented BPW.

158

P. PIem, R. Reissbrodt /ht.

J. Food Microbiology 27 fl995) 147-159

Various techniques can be used to identify Salmonella from swarm zones. A

slide agglutination test performed using a loopful of the migrating cells at the zone
edge and also direct inoculation on selective nutrient media followed by biochemical confirmation have been described (De Smedt et al., 1986). Pless et al. (1993)
reported on the successful use of a latex agglutination test. The present studies
have shown that the C8-esterase reaction employed in the MUCAP-reagent may
be used with both MSRV and DIASSALM media. These media appear to be as
appropriate for this test similar as McConkey agar, reported as the best medium by
Olsson et al. (1989). Pre-enrichment in ferrioxamine E-supplemented Buffered
peptone water for 6 h, preferably with shaking or stirring, followed by motility
enrichment on MSRV or DIASSALM medium for 16-24 h improved detection of
motile Salmonella spp. , also of sublethally injured cells. MUCAP-reagent is used
to confirm that swarming growth on the semi-solid medium is Salmonella. Serological testing is performed to establish the identity of motile serovars.
Further investigations are needed, aimed at determining the suitability of the
method for a wider range of serovars and sub-species. More work is also needed to
confirm the efficacy of ferrioxamine-E supplementation for detecting Salmonella
in mixed bacterial populations, not only by conventional culture methodology, but
also by other methods including rapid test systems.

Acknowledgements

David E. Post, Unipath Ltd., England, is gratefully acknowledged in recognition

of critical reading of the manuscript. The technical assistance of Barbel Burghardt
was greatly appreciated.

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