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Journal of Clinical Microbiology, November 2001, p. 4155-4159, Vol. 39, No. 11
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.11.4155-4159.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Bacterial Genetic Fingerprint: a Reliable Factor in
the Study of the Epidemiology of Human
Campylobacter Enteritis?
B.
Steinbrueckner,1,*
F.
Ruberg,2 and
M.
Kist2
Institut für Labormedizin, Klinikum
Ingolstadt, D-85049 Ingolstadt,1 and
Institut für Medizinische Mikrobiologie und Hygiene,
Universitätsklinikum Freiburg, D-79104
Freiburg,2 Germany
Received 29 January 2001/Returned for modification 11 March
2001/Accepted 11 August 2001
 |
ABSTRACT |
The rate of human intestinal infections with more than a single
Campylobacter strain was determined and the genetic
variabilities of Campylobacter strains throughout an
infection episode were investigated by means of pulsed-field gel
electrophoresis (PFGE) and enterobacterial repetitive intergenic
consensus sequence PCR (ERIC-PCR). For 48 and 49 of 50 patients, all
isolates from one sample showed identical patterns by PFGE and
ERIC-PCR, respectively. Throughout an infection episode in 47 of 52 patients, the PFGE fingerprints of the isolates remained
stable, while in 1 patient two different species were observed and in 4 patients different patterns were observed. Therefore, ERIC-PCR proved
less discriminative than PFGE. These findings suggest that human
infection with more than one Campylobacter strain is
rare and should not significantly impair epidemiologic analyses.
However, changes in the genetic fingerprint throughout an infection
should be considered in the assessment of epidemiologic studies of
Campylobacter spp.
| |
TEXT |
The thermophilic Campylobacter
species, mainly Campylobacter jejuni and Campylobacter
coli, are recognized as important causative agents of acute human
diarrheal disease worldwide. Dogs, cats, and other pets may be a source
of human infection (1). However, Campylobacter enteritis is mainly a food-borne infection.
Healthy food animals, especially poultry, are intestinal carriers of
the organisms, and molecular typing studies have shown that individual birds can harbor up to seven different strains (H. Aarts, E. Bouw, and
B. van Lith, COST Action Workshop on Pathogenic Microorganisms in
Poultry and Eggs, Uppsala, Sweden, p. 14, 1997). Due to the highly automated process in modern poultry slaughterhouses, additional cross-contamination may occur, leading to the isolation of several different Campylobacter clones from one poultry meat product
(5). These findings suggest that most cases of human
food-borne Campylobacter infection might be caused by
several bacterial strains instead of by only one bacterial strain.
In addition to these investigations, many studies have shown a high
degree of genetic heterogeneity among Campylobacter isolates by techniques like arbitrarily primed PCR (10),
enterobacterial repetitive intergenic consensus sequence PCR
(ERIC-PCR) (6), restriction fragment length
polymorphism (RFLP) analysis, mainly of the flagellin gene
(12), and pulsed-field gel electrophoresis (PFGE)
(14). Possible reasons for this heterogeneity are genetic rearrangements due to genomic instability that either occurs
spontaneously or is induced by mobile elements (18);
programmed DNA inversion, as described for Campylobacter
fetus (3); horizontal gene transfer (17); and natural transformation (16). While
some investigators have found evidence for genetic mosaicism or natural
transformation during experimental colonization of chickens
(8), other groups failed to do so (18).
Additional phases that may be candidates for such rearrangements are
during environmental transition or human infection. The study described
here was performed to investigate (i) whether genetically
distinct Campylobacter strains can be simultaneously
isolated from stool samples of patients with Campylobacter enteritis and (ii) whether during an infection episode genetic rearrangements can be observed.
(The results described here were presented in part at the 9th
International Workshop on Campylobacter, Helicobacter and Related Organisms, Cape Town, South Africa, 15 to 19 September 1997.)
Stool samples and bacterial strains.
Human stool samples were
plated on blood-free Campylobacter agar (Oxoid, Basingstoke, United
Kingdom) supplemented with 32 mg of cefoperazone per liter and 10 mg of
amphotericin B per liter. Incubation in all experiments was carried out
for 48 h at 37°C. Jars were partially evacuated and were
refilled with a gas mixture that contained 5%
O2, 10% CO2, and 85%
N2 (final concentrations). Isolates were
identified by standard biochemical tests. To avoid misidentification of
hippurate-negative C. jejuni strains, all hippurate-negative isolates were subjected to previously described PCRs
specific for C. jejuni and C. coli
(4). Subcultures were performed on nonselective
agar plates (yeast-cysteine agar) supplemented with 10%
sheep erythrocytes.
To detect the simultaneous presence of distinct
Campylobacter clones in one stool sample, four individual
colonies were picked from different areas of the original selective
agar and were separately subcultured. Four colonies were chosen for
standardization since more than four colonies can rarely be
discriminated on primary agar plates due to contamination with other
bacteria or fungi, swarming, or low colony counts. To study the
stability of the genetic fingerprint throughout human infection, one
colony per plate was subcultured and analyzed by molecular typing techniques.
Molecular typing.
All isolates were subjected to PFGE and
ERIC-PCR. For PFGE the bacteria were suspended in 0.9% NaCl solution
and were diluted to an optical density of 0.85 at 600 nm. A total of
1.5 ml of this suspension was centrifuged at 15,000 × g for 4 min. The pellet was washed three times and was
resuspended in 0.5 ml of 0.9% NaCl solution. A mixture with 0.7 ml of
1.5% PFGE agarose (Sigma, St. Louis, Mo.) was cast in blocks,
incubated in lysis buffer (0.5 mM EDTA [pH 9.5], 1%
N-lauroyl-sarcosine, 1.8 mg of proteinase K per ml)
overnight, and washed three times in TE buffer (10 mM Tris, 10 mM EDTA
[pH 7.5]). If not otherwise stated, restriction was performed with 20 U of SmaI (New England Biolabs, Beverly, Mass.).
Fragments were separated in a 1% PFGE agarose gel (Sigma) with 0.5×
TBE (45 mM Tris, 45 mM boric acid, 1 mM EDTA) at 200 V and 12°C for
19 h with ramped pulse times from 10 to 30 s in a CHEF DR II
system (Bio-Rad, Richmond, Calif.). In some experiments KpnI (20 U; New England Biolabs) was used as an additional
enzyme, and in this case separation was performed for 12.7 h with
ramped pulse times from 1 to 8 s. Bands were stained with ethidium
bromide, and a 48.5-kb bacteriophage lambda ladder (Bio-Rad) served as a DNA size standard.
DNA for ERIC-PCR was prepared with an extraction kit (Qiagen,
Hilden, Germany), according to the manufacturer's
instructions.
The amount of purified DNA was determined photometrically
on a
GeneQuant system (Pharmacia Biotech, Uppsala, Sweden) and
was
adjusted to a concentration of 20 µg/ml. For the reaction mixture
(final volume, 50 µl),
Taq DNA polymerase buffer
(Pharmacia Biotech)
with 1 mM MgCl
2 and 0.4 µg
of bovine serum albumin was used. Each
primer, primer ERIC 1R and
primer ERIC 2 (
15), was used at a
concentration of 25 pmol. A total of 100 ng of template DNA and
2 U of
Taq DNA
polymerase (Pharmacia) were added to each reaction
mixture. PCR
involved 30 cycles of consecutive denaturation (95°C,
1 min), primer
annealing (40°C, 1 min), and chain extension (65°C,
8 min). Prior
to cycling the samples were heated at 95°C for 7
min. Finally, an
additional extension step (16 min, 65°C) was
performed. A GeneAmp
System 9600 thermocycler (Perkin-Elmer Cetus,
Norwalk, Conn.)
was used. PCR products were separated in 2% agarose
gels and stained
with ethidium bromide.
C. jejuni NCTC 11351 was
included
as a reference strain in each experiment, PFGE, as well
as ERIC-PCR.
All gel images were recorded with an EASY Image Plus
computer based
video documentation system (Herolab, Wiesloch,
Germany). All
band patterns (PFGE and ERIC-PCR) were inspected
and analyzed manually
as well as with a computer. Automated analysis
was performed by the
unweighted pair group method with arithmetic
averages and with
GelCompar software (version 4.0; Applied Maths,
Kortrijk,
Belgium). For the analysis of similarity between the
band patterns, the
Dice coefficient with a position tolerance
of 1.1% was used for the
PFGE patterns and the Pearson coefficient
was used for the more complex
PCR patterns. The existence of double
bands was evaluated by
computer-based densitometry of the individual
bands within a pattern.
Throughout this study, all
Campylobacter isolates were
typeable by PFGE as well as by ERIC-PCR.
Four distinct colonies were picked from the first stool sample
submitted from 50 consecutive patients with
Campylobacter
enteritis,
leading to a total of 200
Campylobacter isolates.
The isolates
of 47 patients were identified as
C. jejuni,
and the isolates
of 3 patients were identified as
C. coli. A
simultaneous infection
with
C. jejuni and
C. coli
was not detected in any patient. A
total of 44 different band patterns
were demonstrated by PFGE.
In 48 of 50 patients the four isolates
exhibited identical band
patterns. Three isolates from one patient
showed identical patterns,
while for the fourth isolate a 409-kb band
was replaced by a 420-kb
band (Fig.
1a). However, when
KpnI was used as the restriction
enzyme, all isolates
exhibited identical patterns (not shown).
In another patient three
isolates showed identical patterns, while
one isolate differed from the
others by seven bands when the band
at 406 kb was considered a double
band, as demonstrated by densitometry
(data not shown) (Fig.
1b).
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FIG. 1.
(a) PFGE patterns for four isolates (lanes 1 to 4, respectively) found in one stool sample of a patient with acute
Campylobacter infection. In lane 1, a 409-kb band was
replaced by a 420-kb band. (b) Four isolates (lanes 1 to 4, respectively) from one stool sample showing two different PFGE
patterns. The pattern for the first isolate differed from those for the
other isolates by seven bands (when the band at 406 kb is considered a
double band, as determined by densitometry). (c) ERIC-PCR patterns for
four isolates (lanes 1 to 4, respectively) found in one stool sample.
The pattern for one isolate (lane 1) differed from the patterns for the
other three isolates, which showed no significant differences. Lanes M,
molecular size markers.
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|
The analysis of the ERIC-PCR patterns showed a total of 44 different
patterns. For 49 of 50 patients the four isolates showed
identical
patterns. For one patient the pattern for one isolate
differed from the
patterns for the other three isolates (Fig.
1c), thus reproducing the
results found by PFGE. The similarity
between those two different
patterns was 51%, and the patterns
for the isolates were the
same those as shown in Fig.
1b.
More than one stool sample from 52 patients was positive for
Campylobacter (2 to 9 samples, with a mean of 2.4 samples)
during
the course of their
Campylobacter infections. The
total number
of isolates was 124, and the interval between the time of
recovery
of the first and the last isolate from each patient was
between
2 and 358 days (mean, 23 days; median, 15 days). All isolates
from 49 patients were identified as
C. jejuni, and all
isolates
from 2 patients were identified as
C. coli. For one
patient
C. jejuni and
C. coli (as proved by PCR)
were detected at an interval
of 25 days. A total of 55 different band
patterns were demonstrated
by PFGE. For 47 of 52 patients, the patterns
for the isolates
obtained by PFGE remained unchanged during the
infection, while
for 5 patients the band patterns for the isolates
changed. In
the case of a 27-year-old immunosuppressed patient, the
initial
isolate exhibited a band at 365 kb, while after 152, 314, and
358 days, a double band at approximately 387 kb was detected for
the
subsequently recovered isolates (Fig.
2a). To confirm this
result an additional
restriction with
KpnI was performed, and
it revealed
identical patterns for isolates 1 to 3 from this patient
and a
pattern for isolate 4 that differed by one band from those
for
isolates 1 to 3 (data not shown). A second stool sample was
obtained from a 7-year-old child 28 days after isolation of
C. jejuni from the first stool sample. Colonies with two different
morphologies were noticed on the primary isolation medium, and
the
isolates in both colonies were identified as
C. jejuni. The
band pattern for the smaller colonies exhibited a double band
at 361 kb
and differed from the pattern for the previous isolate
by two bands,
while the band pattern for the larger colonies differed
from that for
the previous isolate by four bands. The patterns
for the small and the
large colonies differed by six bands (Fig.
2b). Two patterns for the
C. jejuni isolates obtained from a 27-year-old
man within an
interval of 7 days exhibited a difference of seven
bands when the band
in lane 2 (Fig.
2c) at 327 kb is considered
a double band, as
demonstrated by densitometry (data not shown).
Two isolates were
obtained within an interval of 33 days from
a child 21 months of age.
The patterns for these isolates differed
by six bands if the bands at
343 kb (lane 1) and 164 kb (lane
2) are considered double bands (Fig.
2d). For a 23-year-old patient,
a second isolate that was identified as
C. coli was isolated 25
days after the isolation of
C. jejuni. The patterns for the isolates
of the two species differed
by 12 bands (Fig.
2e). All isolates
from the five patients that
exhibited different PFGE patterns
during the course of infection
were also typed by ERIC-PCR. By
ERIC-PCR the isolates from one
patient that differed by two bands
by PFGE (Fig.
2b, lanes 1 and
2a, respectively) exhibited identical
patterns. Also, the three
isolates from one patient with different
colony morphologies and
with PFGE patterns that differed by two
to six bands had identical PCR
patterns. The three pairs of isolates
whose patterns differed by 6 to
12 PFGE bands showed distinct
PCR patterns, with similarities of
89, 56, and 38%, respectively
(Fig.
3).
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FIG. 2.
(a) PFGE patterns for four isolates from four different
stool samples of a 27-year-old immunosuppressed male. Lanes 1 to 4 show
the patterns for the isolates obtained at the first examination and
152, 314, and 358 days after the first examination,
respectively. The pattern for the initial isolate exhibited a
band at 365 kb, whereas the other isolates showed double bands at 387 kb. (b) Isolates collected from two samples of a 7-year-old child. Two
isolates from the second sample with small and large colony
morphologies (lanes 2a and 2b, respectively) were detected. The PFGE
patterns for all three isolates differed from each other. (c) PFGE
patterns for two isolates obtained from a 27-year-old male showing a
difference of seven bands with a double band at 327 kb. (d) Isolates
collected from a 21-month-old child. The PFGE patterns differed by six
bands, with the bands at 343 kb (lane 1) and 164 kb (lane 2) considered
double bands. (e) Different PFGE patterns for two isolates obtained
from a 23-year-old male and identified as C. coli (lane
1) and C. jejuni (lane 2).
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FIG. 3.
ERIC-PCR patterns for those isolates that exhibited
different PFGE patterns during the course of infection. Weight markers
(lane M) and the pattern for a negative control (lane 0) are also
shown. All isolates with PFGE patterns that differed at 6 to 12 bands
also had different PCR patterns. Lanes 5 and 6, lanes 10 and 11, and
lanes 12 and 13 correspond to the lanes in Fig. 2d, c, and e,
respectively. Isolates with PFGE patterns that differed by two to six
bands had identical PCR patterns. The PCR patterns in lanes 1 to 4 correspond to the PFGE patterns in Fig. 2a, lanes 1 to 4, respectively.
The PCR patterns in lanes 7 to 9 correspond to the PFGE patterns in the
three lanes in Fig. 2b, respectively.
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|
C. jejuni NCTC 11351 was included in each experiment
as a reference strain. In all experiments the patterns for this
strain
clustered with similarities of at least 84 and 80% with the
patterns
in the PFGE and PCR databases, respectively.
Therefore, in the
computer-based analysis all PFGE and ERIC-PCR
patterns that clustered
with similarities higher than 84 and 80%,
respectively, were considered
identical. Those clusters of
patterns considered identical by
computer-based analysis were
additionally checked by visual comparison.
Since ERIC-PCR amplicons
smaller than 300 bp and larger than 1,700
bp had poor reproducibilities
while amplicons within this size
range had high reproducibilities, only
bands between 300 and 1,700
bp were
analyzed.
Tracking the sources and routes of infection in outbreak situations
and, even more interestingly, in sporadic cases of infection
is based
to a large extent on analysis of genetic markers and
molecular
fingerprinting methods. All these strategies depend
on two major
preconditions: (i) the exclusive presence of the
investigated clone of
a certain species in the putative source
as well as in the infected
individual and (ii) the stability of
the distinctive molecular
characteristics used as epidemiologic
markers in a defined bacterial
clone. For epidemiologic studies
of human
Campylobacter
infections, neither of these two conditions
has yet been unequivocally
proven. In contrast, the isolation
of multiple
Campylobacter
strains from single sources of infection
(Aarts et al., COST Action
Workshop on Pathogenic Microorganisms
in Poultry and Eggs) and the
presence of genotypic variation within
single
Campylobacter
clones, as demonstrated by RFLP analysis
of the flagellin gene
(
9) and as detected even more reliably
by PFGE (
17,
18), have raised substantial doubts concerning
these
preconditions (
13). The appearance of 55 and 44 different
band patterns by PFGE and ERIC-PCR, respectively, in the
Campylobacter isolates from a total of 50 patients from a
restricted geographic
area proved the high discriminatory powers of
both of these methods
for the typing of
Campylobacter spp.
For isolates from 96% of
the patients, a single band pattern was
exclusively obtained by
both typing techniques. For the isolate from
one patient (Fig.
1a), a difference in the PFGE pattern of only two
bands at least
indicated a strong genetic relation between the
isolates. Even
more, the difference might be interpreted as the
mobility shift
of one band for identical isolates. This assumption was
supported
by restriction with
KpnI and ERIC-PCR, which did
not discriminate
between the two isolates. The PFGE band patterns from
various
isolates from one stool sample from only one patient differed
by seven bands, indicating genetic diversity. This finding suggests
that human
Campylobacter infection most frequently is due to
a
single bacterial clone. This finding is somewhat surprising in
light
of the previously described contamination of putative sources,
i.e.,
poultry, with more than one clone (
5). A possible reason
for this discrepancy might be differences in the pathogenicities
of
food-contaminating strains, with only certain strains being
able to
establish infections in humans. Furthermore, different
growth demands
could lead to the overgrowth of a single strain.
The preparation of
food could also result in the selection of
one strain. Improper cooking
of chicken meat might lead to killing
of superficially contaminating
bacteria, while a strain in the
inner parts of the food would be
exposed to lower temperatures,
thus being able to survive. Finally,
those results could be explained
by overestimation of poultry meat as a
source of infection since
simultaneous contamination with different
strains has been demonstrated
to a much lesser extent for other sources
like raw milk and drinking
water (
7,
11). However, this
subject has not been studied
in
detail.
The second part of the study focused on a further prerequisite of
epidemiologic investigations, namely, the stability of the
genetic
fingerprint of
Campylobacter. For 90% of the patients,
a
single bacterial genetic fingerprint was detected by PFGE throughout
the course of a
Campylobacter infection. For 10% of the
patients,
however, the band patterns for the isolates changed during
the
infection episode. In one patient (Fig.
2e) the difference was
probably due to a coinfection or a reinfection since the two isolates
detected within an interval of more than 3 weeks were identified
as
C. jejuni and
C. coli, respectively. Underlining
the lack of
genetic relatedness of these two isolates, the PFGE
patterns differed
by as many as 12 bands. For isolates from four
patients (Fig.
2a to d), two to seven different bands in the patterns
for the
Campylobacter isolates obtained during the course of
infection
could be observed by PFGE. For one patient (Fig.
2a) an
additional
difference was detected by the use of a second restriction
enzyme.
Interestingly, the isolates that differed by less than six
bands
by PFGE could not be discriminated by ERIC-PCR, while isolates
that differed by more than six bands by PFGE also showed distinct
ERIC-PCR patterns. These findings underline the high degree of
discriminatory power of PFGE for the typing of
Campylobacter
spp.
and support the recommendation that more than a single typing
technique should be used for epidemiologic studies (
2).
Due
to the design of this study, it cannot definitely be
determined
whether the genetic differences in
Campylobacter isolates obtained
during the course of an
infection were due to genetic changes
or to a coinfection or a
reinfection. With regard to the first
part of the investigation, in
which the simultaneous detection
of distinct genotypes was very rare,
however, genetic instability
is more probable. This instability was
associated with the acquisition
of DNA of approximately 22 kb (Fig.
2a), 40 kb, and 70 kb (Fig.
2b). For the isolates from two patients
with differences of six
(Fig.
2d) or seven (Fig.
2c) bands, the
mechanisms of acquisition
or loss of DNA and the simultaneous
rearrangement or acquisition
of point mutations are much more complex,
and several causative
genetic events would be possible. To exclude the
possibility that
these strains had high-grade genetic instability, they
were serially
passaged in vitro 45 times on nonselective medium. The
PFGE patterns,
however, remained unchanged (data not
shown).
In conclusion, simultaneous infection with more than one
Campylobacter strain seems to be a rare event and therefore
does
not remarkably impair genotypic analysis of epidemiologic
patterns.
However, during an infection episode the causative
Campylobacter strain can undergo substantial genetic
changes. This must be taken
into account for future epidemiologic
investigations. Otherwise,
misinterpretation of data by underestimation
of epidemiologic
relations might be the
consequence.
| |
ACKNOWLEDGMENTS |
We thank Marianne Vetter-Knoll and colleagues of the stool
laboratory at the Institut für Medizinische Mikrobiologie und Hygiene for skillful assistance.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Institut
für Labormedizin, Klinikum Ingolstadt, Krumenauerstr. 25, D-85049
Ingolstadt, Germany. Phone: 49 (841) 880 2904. Fax: 49 (841) 880 2912. E-mail: bernhard.steinbrueckner{at}klinikum.ingolstadt.de.
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| 18.
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Wassenaar, T. M.,
B. Geilhausen, and D. G. Newell.
1998.
Evidence of genomic instability in Campylobacter jejuni isolated from poultry.
Appl. Environ. Microbiol.
64:1816-1821[Abstract/Free Full Text].
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Journal of Clinical Microbiology, November 2001, p. 4155-4159, Vol. 39, No. 11
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.11.4155-4159.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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