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Detection
and enumeration
of Salmonella
and Pseudomonas
aeruginosa
Bernard
and Harold
A. Kenner
P. Clark
Federal
Pollution
Water
Con
Amendments
of
19721_4
may
The
well
the quantification
and enu
require
meration
of pathogens
such as Salmonella
in all classes of waters.
The re
species
are
described
Shedroff.5
quirements
by
One of the continuing
of the
programs
Environmental
Protection
Agency
(epa)
is a research project
concerned
with
the
of practical
meth
development
laboratory
ods for the isolation,
and
quantification,
enumeration
of pathogens
from polluted
waters.
This paper reports a monitoring
method
for the simultaneous
developed
isolation
and enumeration
of Salmonella
from
species and Pseudomonas
aeruginosa
trol
potable
waters,
reuse
waters,
treatment
and
waters,
effluents,
plant
receiving
sludges.
The method
and de
described
herein,
is
because
Kenner,6
veloped
by
practical
available
media,
readily
bacteriological
are all that are
and equipment
chemicals,
to obtain
the desired
results.
required
These
results are the establishment
of the
or presence
absence
of Salmonella
species
hazardous
bacteria ) and/or
(pathogenic
Pseudomonas
aeruginosa
patho
(potential
are in a
that affect persons who
gens)
debilitated
condition
and are very com
mon
as infectious
in hospitals
be
agents
cause
of
to antibiotic
their
resistance
Potable waters have also been
therapy.7-9
shown
sources
human
waters.11'
to
contain
Ps.
aeruginosa.6'10
The
are
of these potential
pathogens
and
animal
feces
and waste
12
When
the monitoring
method was used,
it was found that 100 percent of municipal
wastewaters
and treatment
plant
sludges
contained
both of these potential
patho
Ps.
has been
found in
gens.
aeruginosa
potable water
supplies of large and small
insufficient
where
residual
municipalities
is evident.
is the
chlorine
Also important
fact that these organisms may be found in
of fecal coliforms,
the absence
whereas
tests
indicator
may
negative
give a false
sense of security.
It is believed
by the
authors that these organisms may be better
indicators
than fecal coliforms
of pollu
tion in potable,
direct reuse, bathing,
and
waters.
recreational
and
Materials
Methods
uses a multiple
The monitoring
method
tube
in
which
dulcitol
(mpn) procedure
13 is
selenite broth
used
for
primary
(dse)
enrichment
and is modified
medium,
by
acid
the use of sodium
selenite
(bbl).
The formula is proteose
peptone
(Bacto),
extract
0.4 percent;
0.15
yeast
(Bacto),
0.4 percent;
0.5
bbl,
dulcitol,
percent;
0.125
and
Na2HP04,
percent;
percent;
in distilled water.
0.125 percent
KH2P04,
are dissolved
in a sterile
The constituents
to
flask, covered with
foil, and heated
88 ?C in a water
bath to obtain a clear
sterile medium
that does not require ad
of
for Salmo
justment
pH.
Productivity
nella species is enhanced
addition
the
by
of an 18-hr, 37 ?C culture
of Salmonella
A (10 percent
in
paratyphi
by volume)
dse broth, killed by heating
single-strength
to 88?C.
Concentration
from
of bacteria
large
volumes
of
water
is necessary
reuse,
ble, direct
treatment
effluents
-Vol.
46, No.
when
pota
and
waters,
receiving
are being monitored.
9, September
1974
2163
and Clark
Kenner
TABLE
of Several
Characteristics
I.?Retentive
Compared
with
Filter
Filter,
Corp.
47 mm,
47 mm,
Glass
GF/D
Paper Whatman,!
Reeve
Angel
Corp.
934AH
47 mm,
Fiber Filter,
Glass
Reeve
Angel
Corp.
47 mm,
Glass
GF/A
Paper Whatman,
Percentage
Retention
Angel
Corp.
984H
Ultra
Glass
Fiber
Filter
is flexible
when
paper
filter GF/F
1,376
100
1,229
25
98
2,698
has better
retentive
99.8
17.4
2,166
2,622
can
Oct.
Papers*
47 mm,
Glass
GF/F
Paper Whatman,t
Reeve
Angel
Corp.
The
Filter
Millipore
Fiber
Number Passing
Filter
Total Bacteriaf
Filtered
Filter
Reeve
Glass
Filters
Membrane
1,049
198
81
1,066
680
36
wet,
placed
properties
than
the 984H,
of
large volumes
broth,
and has
same
disintegrates
properties
of water,
when
(tested
1973).
is attained
filtration
by
*
fiber
in a membrane
filters
through glass
filter apparatus.
After the desired volume
of water
is filtered through the ultra filter,
Concentration
2164
&< Co.,
N.
Inc., Clifton,
J.
not
en
does
constitute
names
or recommendation
by EPA.
of 40? ? 0.2?C
Incubation
temperature
for 1 and 2 days is critical to obtain opti
mum
of
Salmonella
sp. and
recovery
dse broth
when
Pseudomonas
aeruginosa
is used
After
for primary
enrichment.
at 40? C, surface loop
incubation
primary
or nichrome
fuls (scum)
(7 mm platinum
are
each multi
wire
removed
from
loop)
on each of
and
culture
streaked
ple-tube
two sections of a divided
plate of Xylose
15 in
order
agar (xld)
lysine desoxycholate
to isolate colonial growth.
The numbered
at 37 ?C
plates are inverted and incubated
for a period not to exceed 24 hr.
xld agars (bbl
Commercial
dehydrated
are satisfactory
if they are re
and Difco)
in sterile
in distilled
water
constituted
to 88? or
flasks and heated
foil-covered
is then
92 ?C, respectively.
The
agar
in
to 55? to 60 ?C and distributed
cooled
This
sterile petri dishes.
laboratory pre
in each section of a
fers 10-ml portions
divided
(Figure
sterile
disposable
1).
Journal WPCF
plastic
dish
Pathogen
i
Sterile
polypropylene
container
Detection
Filter funnel
for 47-mm 984 H
filter pad
n
for
10-liter
test
vacuum
flask
1000ml pad
1xDSE broth
into 20ml
inserted
for each of 5-tubes
row
1st
^_
Jn
2ml to
8ml 1xDSE in
2nd row
is
After filtration filter-pad
folded double with forceps
4
1ml from
2nd row to
9ml 1xDSE
^3rd row etc.
MPN incubated at 40C for
^Completed
medium
streaked
for
1- and 2- days-Secondary
from surface MPN tubes with
isolated colonies
22 gauge
7 mm Nichrome
loop
6
Loosen
invert plates
incubate
37C
hrs
20-24
Loosen
caps
HI
Chloroform
extract
blue
FIGURE
Positive
incubated
contain
clear,
typical
centered
Salmonella
xld
40C
I1000A
King A
Tech Agar
1.?Procedure
cultures
plate
black
pink-edged,
and
colonies,
flat,
mucoid,
grayish alkaline, pink erose-edged
Ps. aeruginosa.
The Salmonella
colonies
are picked
or
to Kligler
iron agar (kia)
iron
slants
for
agar
sugar
Triple
typical
for isolation
of pathogens.
46, No.
9, September
1974
2165
and Clark
Kenner
TABLE
of Ultra-filter
984H
for Salmonella
IL?Advantage
Use
Waters
Type
5.
4.5
runoff
Stormwater
Serotypes Found
(no./100 ml)
Salmonella
(no./100 ml)
of Sample
in Monitoring
Suspected
species
Salmonella
(no./gal)
210
bareilly1
Serotypes Found
(no./gal)
S.
kottbus10
S.
sludge effluent
wastewater
<3.0
Municipal
Municipal
wastewater
<3.0
Activated
sludge
Activated
7.3
<3.0
runoff
Stormwater
3.6
6.2
Arizona3
1,500
110
bareilly11
S. java*
S. muenchen2
S. group G4
Arizona4
S. anatum2
S. newport4
S. san diego1
S. worthington2
S. anatum3
S. derby1
S. newport3
River
Mississippi
403.1
mile
Municipal
43
water,
28
none
<3.0
effluent
S.
> 11,000
ohio10
S.
blockley1
S. newport3
S. ohio19
S. derby2
S. meleagridis*
S.
3.0
wastewater
21
cholerasuis
var. kunzendorf2
S.
cholerasuis
var. kunzendorf5
5.
or alka
night at 37 ?C, give an unchanged
is
line red-appearing
the
butt
black
slant;
ened by H2S, is acid-yellow,
and has gas
bubbles,
except for rare species.
Typical
are purified
slant cultures
appearing
by
them to xld agar plates
for
transferring
the development
of isolated colonies.
The
flat or umbonated-appearing
colonies with
and clear pink edges
large black centers
then are picked to kia slants ( streaked and
at 37?C,
incubated
stabbed),
tested before
the identification
and
urease
procedure
tubes are re
1). Urease-negative
tests
for presumptive
serological
and serotype
identification.
Tech agar slant cultures for Ps.
Typical
at 40?C
that are incubated
aeruginoca
a
turn
color
from
overnight
bluegreen
(Figure
tained
pyocyanin,
this species.
a pigment
produced
A reddish-blue
color
only by
is caused
of pyorubin.
presence
by the additional
is extractable
in chloro
The blue pigment
form and is light blue in color after a few
hours at room temperature.
No
further
tests are necessary.
rectly from the mpn
2166
The
table.
count
is read di
Justification
for
newport*
Procedures
Choice
of primary
enrichment
medium
and secondary
isolation agar. Most of the
in contem
enrichment
media
described
were
literature
for the
porary
designed
isolation of pathogens
from clinical
speci
mens
from ill persons or from samples of
foods, and they work quite well
suspected
for those types of samples.
When
they
are used, however,
for the isolation
of
from polluted
pathogens
types of environmental
waters
and other
such as
samples,
En
soils, they do not prove
adequate.
richment media that were tested and found
in regard to detection
and selec
wanting
tetrathionate
tivity were
and without
brilliant
selenite
(tt), with
at
41.5 ?C;
green
at 37?C;
selenite
broth
broth
cystine
at 37?C; selenite brilliant
green,
with and without
sulfa, at 37? and 41.5?C;
and Gram-negative
broth
(gn) at 40? and
F broth
41.5?C.
Journal WPCF
Pathogen
TABLE
No.
Liquid Samples
wastewater
Municipal
Stockyard
Rivers
of Colony Picks
for Salmonella
III.?Percentage
wastewater
Ohio
Activated
sludge
effluent
110
18
84
14
26
76
78
386
103
83
41
17
306
78
55
37
13
80
37
17
16
10
21
20
16
14
80
15
78
66
13
65
9
189
3
155
6
2
2
plant
package
cisterns
R-0
Dupont
outfall
2
2
Home
Feed
Reject
Product-negative
Raw
sludge
primary
4
sludge
digester
sludge
digester
sludge
activated
(28 days)
Activated
secondary
Total
biological
20
sludge
6
84
1,223
28
4
4
2,100
2
13
3-43
4.5-12
0.26-1.1
4.3
0.91
13-700
23
79-170
33
82
6
34
average
1.5
1.8-620
83
87
83
14
>300
43-240
70
50
1.5
0.2
0.1-1,100
0.35-140
43
59
347
3.0-1,500
79
76
66
90
76
25
1,570
Range of
Salmonella
counts/100 ml
Percentage
Positive
79
100
Package
plant effluent
sludge
Package
plant
outfall
Chlorinated
primary
Anaerobic
No.
Negative
65
0
Primary
Anaerobic
No.
Positive
Total Picks
from xld
250
36
Creek 1mile
Positive
315
36
runoffs
Combination
species
15
1
Mississippi
Stormwater
from DSE-XLD
Detection
ll->
11,000
78
reasons
of tt,
for rejection
The main
and
for
brilliant
and without
with
green,
selenite broth's using brilliant
agar
green
are not
and xld agar as secondary media
sp., but
only fewer isolations of Salmonella
of these combina
also the poor selectivity
tions when
they are used for monitoring
waters.
These combinations'
poor
polluted
at
in the
41.5
?C is apparent
selectivity
results of Dutka
and Bell,18 where
the tt
26 percent
broth-xLD combination
yielded
confirmation
of colonial picks, and selenite
broth-BGA and selenite broth-XLD gave 55
and 56 percent
confirmations,
respectively.
The authors had similar results.
The gn
xld
was
water
combination
for
poorest
less
samples at 40? and 41.5?C, yielding
than 10 percent
isolations
from waste
waters.
on iso
Effect of incubation
temperature
a
In
lation of Salmonella
sp.
study of
was
26 wastewater
that
conducted
samples
with
the dse multiple
tube setups at three
-Vol.
46, No.
9, September
1974
2167
and
Kenner
TABLE
Clark
IV.?Serotypes
Polluted
1 typhimurium*
2 derby
3 cubana
4 ehester
5 newport
6 kottbus
7 blockley
8 infantis
9 enteritidis
10 anatum
11 Heidelberg
12 manhattan
13 paratyphi B
14 illinois
15 thornpson
16 livingstone
17 montevideo
18 muenchen
19 oranienberg
20 saw ?tego
21 barielly
22 tshiongwe
23 orion
24 senftenberg
25 schwarzengrund
26 lexington
27 cholerasuis
28 fcittsa
29 cholerasuis var.
kunzendorf
Salmonella
Found
in
Waters
No. of
Strains
Serotype
Other serotypes
30 albany
31 benfica
32 braenderup
33 brancaster
34 bredeney
35 california
36 dry Pool
37 friedenau
38 gw
39 grumpensis
40 ?fli/a
41 Hartford
42 Havana
43 indiana
44 java
45 javiana
46 litchfield
47 lomita
48 meleagridis
49 mission
50 newington
51 newlands
52 norwich
53 oftt'o
54 preston
55 reading
56 rubislaw
57 sainf ?)awi
58 schleissheim
59 simsbury
60 taksony
61 tennessee
62 typhi-suis var.
voldagsen
63 uzaramo
64 ??>?7
65 worthington
of
375
287
223
203
188
158
157
141
128
127
110
97
91
77
63
52
47
45
44
44
42
41
41
39
37
33
30
29
Rank in
Water
Isolations
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
19
20
21
21
22
23
24
25
26
29
:
Sub total
Arizona
Incomplete serology
Total
* Rank
20
10
13
1
8
2
14
4
25
10
2
2
16
10
15
13
17
26
18
14
2
8
14
19
2
26
15
21
12
9
16
12
2
28
3
10
31
40
38
Results
37
29
40
35
40
36
38
34
28
33
37
37
32
28
36
30
39
35
39
27
40
3,417
151
232
3,800
2168
it was
found that
different
temperatures,
of the samples contained
Sal
100 percent
at 40?C.
monella
sp. and Ps. aeruginosa
At 41.5?C, however,
only 50 percent or 13
of the samples yielded
Salmonella
sp., and
at 37 ?C only 8 percent or 2 of the samples
sp.
yielded Salmonella
Effect of enhancement
of dse broth with
a killed culture of S. paratyphi
A.
In a
84
of
activated
of
sludge
samples
study
effluents,
trickling filter effluents, package
dse
and stream waters,
effluents,
plant
a killed
broth enhanced
culture
with
of
A in dse broth
S. paratyphi
(10 percent
in 64 sam
isolations
by volume)
yielded
isolated Salmonella
sp.,
ples or 74 percent
48 samples or 57 percent
compared with
isolations when
the dse broth was
used
iso
An improved
without
enhancement.
lation of 17 percent was
achieved
with
enhanced dse broth.
Ultra-filter.
of ultra
The
advantages
filter use in testing water
samples are illus
trated in Table II.
and
Discussion
use
to those who must
importance
to
tests
Salmonella
obtain
bacteriological
Of
sp.
and
Ps.
aeruginosa
counts
from
waters
Journal WPCF
Pathogen
TABLE
of Various
V.?Percentage
Type
Before
chlorination
After
chlorination,
5 min
residual,
filter
Package
plant
1 mile
Creek
Ohio
plant
River
Wabash
Septic
effluents
effluents
(1.6 km)
below
Cincinnati
28
40
29
11
26
15
11
15
public
after
heavy
rain
suburban
cisterns
tank sludges
20
1*
31
11
18
13
6
4
3t
0
3?
4
114
69
183
Totals
Municipal
f Positive
? Negative
Number
Negative
0
above
collective
runoff
species
package
River
Stormwater
Farm wells
Number
Positive
for Salmonella
mg/1
landing
River
Mississippi
Streams
Home
1.4-2.0
contact
Positive
Samples
28
effluents
primary
Municipal
(chlorinated)
effluents
Activated
(clarified)
sludge
effluents
Activated
sludge
Trickling
of Water
Number of
Samples
of Sample
wastewaters
Municipal
Types
Detection
intake.
technique.
by per-gallon
by per-100 ml technique.
concentrate
in a 10-gal (38-1)
the bacteria
or
a
of
(380-1)
sample
100-gal
sample
or
reuse
to
water
obtain
results,
potable
and still not require even more expensive
or centrifugation
filtration
It
equipment.
to test only extremely
also seems unrealistic
small samples of the water being examined,
because
they may not be representative.
a list of Salmonella
IV contains
Table
serotypes isolated from polluted waters and
ranked according
to the frequency
of sero
It will be noted
that all
type isolations.
of the serotypes
iso
except S. typhi were
lated from environmental
samples by the
and
that
method,
monitoring
only 6 of the
65 serotypes
were
not reported
reported
as occurring
in humans
in the U. S. over
the period from 1965 to 1971.
Table V summarizes
the percentage
of
various
water
of
types
positive
samples
for Salmonella
sp. Of interest is the fact
that 100 percent
of the municipal
waste
waters
tested contain Salmonella
sp., that
56 percent of chlorinated
primary effluents
tested contain the pathogens,
and that 100
of chlorinated
effluents
percent
secondary
are negative
are
for pathogens.
There
more
studies scheduled
for testing of sec
to obtain
and tertiary
effluents
ondary
et
minimal
chlorine
residuals.
Calabro
that more
than 50 attempts
al.20 reported
at isolating Salmonella
sp. from septic tank
samples
using
sbgs-bgsa
combinations
were
unsuccessful.
VI
summarizes
of
Table
the isolation
Ps. aeruginosa
from potable water
supply,
that is, wells,
cisterns, and small municipal
water
It should be noted
that
supply.
in most
fecal coliforms were not detected
of these samples.
Fecal streptococci
counts
were
than
counts
fecal
coliform
higher
where both tests were used.
Ps. aeruginosa
were present
in all but three of the tests,
and Salmonella
from
isolated
sp. were
two different
cistern samples.
It is of importance
to the user of patho
In
gen tests that the test be quantitative.
initial studies on the dse-xld
combination,
it was important to know if the enrichment
broth would
support the growth of a wide
-Vol.
46, No.
9, September
1974
2169
Kenner
and
Clark
TABLE
Type
Well
Well
Well
Well
of Pseudomonas
VI.?Isolation
Ps. aeruginosa
Isolation
of Sample
8/16/71
8/25/71
3/27/72
3/27/72
Suburban
8/23/72
10/ 4/72
+
+
22
Population
Fecal
Coliforms
0.25
<2
180
15
<2
<2
3
supplies
served
54,700
served
<1
<1
<1
+
+
+
+
0.26
+
0
<1
<1
<1
14,000
<
served
<1
+
10,000
11/27/72
sp. also
<1
present
in samples.
range of Salmonella
serotypes.
Laboratory
cultures of S. paratyphi A, S. typhimurium,
S. bredeney,
S. oranienberg,
S. pullorum,
S.
S. give, and S. worthington
were
anatum,
in three enrichment
tested
broths.
The
time required to isolate each of the above
cultures from an estimated
10 to 20 orga
in
was 48 to 72
ml
water
buffer
nisms/100
hr for S. paratyphi A in tt broth, 24 hr for
dse broth, and 36 to 48 hr for sbgs broth.
The rest of the cultures were
isolated in es
timated numbers
in 14 to 24 hr in tt and
dse broths.
In sbgs broth, S. typhimurium?,
S. bredeney,
S. anatum,
S. give,
and S.
worthington
required 36 to 48 hr incuba
and S. oranienberg
tion, and S. pullorum
required 48 to 72 hr incubation.
It is impossible
to know if 100 percent
of Salmonella
water
sp. in a polluted
are
In
tests
isolated.
where
lab
sample
2170
ml
<1
5/ 8/72
10/24/72
Salmonella
Indicators/100
<1
+
+
3/17/71
6/21/71
7/19/71
6/19/72
10/ 9/72
5/ 8/72
Supply
cisterns
Municipal
Population
Water
8/ 4/72
10/ 9/72*
11/ 6/72*
11/ 6/72
11/26/72
Population
Total
Coliforms
(chlorinated)
Well
Well
from Potable
aeruginosa
in low
oratory cultures have been added
to wastewater
numbers
and
treatment
effluent samples, all of the numbers added
were detected,
as well
as the Salmonella
The
sp. that were
occurring.
naturally
of the water
the quality
higher
(for ex
or tertiary
treatment
ample,
secondary
or
even
the
better
effluent,
potable waters),
the possibility
pf isolation of all the Salmo
as well
as Ps.
nella
serotypes
present,
a potential
aeruginosa,
pathogen.
Summary
A practical
is pre
laboratory method
sented for the simultaneous
and
isolation
enumeration
of Salmonella
sp. and Pseudo
monas aeruginosa
from all classes of waters,
a
including
potable water
supplies, with
minimum
of interfering
false positive
iso
lations. The method
allows for the testing
JournalWPCF
Pathogen
of large volumes
of high quality waters,
the absence of indicator bacteria
wherein
fecal coliforms,
is, total coliforms,
(that
and fecal streptococci),
may give a false
sense
low
of the
of security
because
tested.
of water usually
volumes
Justifica
tion for each step of the procedural method
is
presented.
7. Moody,
M. R.,
in a Center
et
al, "Pseudomonas
for Cancer
Research.
tribution
of
Human
and
Intraspecies
Environmental
1. Federal
PL
Water
Pollution
86 Stat.
Control
816,
33
Amendments,
U.
S. Code
Assurance
Monitoring,
III.
Analysis
for
Salmonella
U.
Tool."
10. Reitler,
monas
of Waste
S.
Research
species
EPA,
Center,
Treatment
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a Surveillance
as
National
Cincinnati,
Environ
Clin.
Lab.
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11. Ringen,
L. M.,
and Drake,
C. H.,
"A Study
of the Incidence
of Pseudomonas
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from
Various
Natural
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64, 841
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12. Drake,
for
C.
the
(1952).
"Evaluation
H.,
of Culture
and
Isolation
Pseudomonas
Media
Enumeration
of
Health
aeruginosa."
Lab.
Sei., 3, 10 (1966).
13. Raj, H.,
"Enrichment
Medium
of
Salmonella
from
Fish
"Standard
Water
for
Methods
the
for
Examination
of
13th Ed.,
Amer.
York, N. Y. (1971).
of
I.
Shigellae.
and Wastewater."
Health
Assn., New
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15. Taylor,
W.
"Isolation
I.,
New
Xylose
Lysine
Agars;
lation
of Enteric
Pathogens."
W.
Isolation
of
Read,
in
R.
B.,
Jr.,
Iso
Bull.
Salmonella
and
for
Tech.
Stokes,
Brilliant-Green
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W.,
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14, 12 (1966).
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Office
of Research
Division,
1st
U.
S. EPA,
"Proc.
on
Seminar
Standardization
Microbiology
of Methods."
EPA-R4-73-022
(Mar. 1973).
B. A., et al, "Simultaneous
6. Kenner,
Quantita
tion of Salmonella
and Pseudomonas
species
I. Polluted
II. Persist
Waters.
aeruginosa.
ence
in Sludge
of Pathogens
Treated
Soils.
mental
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(Eli Lilly),
92-500,
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"Epidemiology
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Sur
aeruginosa
veillance
by a Combined
Typing
System."
Acknowledgments
References
from
Types
Sources."
et al,
P.,
Pseudomonas
assistance
of
Credits.
The
technical
in performing
the neces
Pauline C. Haley
for identifying many
of the
sary serology
is gratefully
Salmonella
serotypes
reported
acknowledged.
is super
Bernard A. Kenner
Authors.
and
Harold
research
microbiologist,
visory
is biological
P. Clark
technician, Waste
and Analysis Activity
of the
Identification
Treatment
Advanced Waste
Research Lab
Research
Environmental
oratory, Natonal
S. Environmental
Protection
U.
Center,
Ohio.
Agency, Cincinnati,
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Inf. Diseases,
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monas
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2171