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Journal of Clinical Microbiology, August 2001, p. 3002-3005, Vol. 39, No. 8
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.8.3002-3005.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Automated Ribotyping Using Different Enzymes To
Improve Discrimination of Listeria monocytogenes Isolates,
with a Particular Focus on Serotype 4b Strains
Alessandra
De Cesare,1
James L.
Bruce,2
Timothy R.
Dambaugh,2
Maria E.
Guerzoni,1 and
Martin
Wiedmann3,*
University of Bologna, Bologna,
Italy1; Qualicon Inc., Wilmington,
Delaware2; and Department of Food
Science, Cornell University, Ithaca, New York3
Received 18 December 2000/Returned for modification 12 February
2001/Accepted 8 April 2001
 |
ABSTRACT |
To develop improved automated subtyping approaches for
Listeria monocytogenes, we characterized the discriminatory
power of different restriction enzymes for ribotyping. When 15 different restriction enzymes were used for automated ribotyping of 16 selected L. monocytogenes isolates, the restriction enzymes
EcoRI, PvuII, and XhoI showed high
discriminatory ability (Simpson's index of discrimination > 0.900) and produced complete and reproducible restriction cut patterns.
These three enzymes were thus evaluated for their ability to
differentiate among isolates representing the two major serotype 4b
epidemic clones, those having ribotype reference pattern DUP-1038 (51 isolates) and those having pattern DUP-1042 (20 isolates). Among these
isolates, PvuII provided the highest discrimination for a
single enzyme (nine different subtypes; index of discrimination = 0.518). A combination of PvuII and XhoI showed
the highest discriminatory ability (index of discrimination = 0.590) for these isolates. A group of 44 DUP-1038 isolates and a group
of 12 DUP-1042 isolates were identical to each other even when the
combined data for all three enzymes were used. We conclude that
automated ribotyping using different enzymes allows improved discrimination of L. monocytogenes isolates, including
epidemic serotype 4b strains. We furthermore confirm that most of the
isolates representing the genotypes linked to the two major
epidemic L. monocytogenes clonal groups form two
genetically homogeneous groups.
| |
TEXT |
Listeria monocytogenes is
a pathogen that causes a severe human food-borne disease
(26). Molecular subtyping provides a crucial tool for the
detection of human listeriosis outbreaks and single-source clusters,
which are often difficult to detect by classical epidemiological
methods without molecular subtyping-based surveillance data. Clinical
characteristics of human listeriosis complicating the detection and
tracking of outbreaks include a long incubation period (1 to 90 days)
in comparison to that of many other food-borne diseases. L. monocytogenes has also been shown to persist in food plants and
thus can lead to prolonged contamination of food products, which may be
distributed over a wide geographic range. As a consequence, this
organism may cause widespread multistate and possibly multicountry
outbreaks, with relatively few related cases in each geographic area.
Rapid and standardized subtyping methods for L. monocytogenes are thus particularly important for effective
detection of human listeriosis outbreaks.
Various methods can be used to distinguish L. monocytogenes
subtypes. Traditional subtyping methods include serotyping
(34) and phage typing (23, 24). Serotyping is
of restricted value because most human clinical L. monocytogenes isolates belong to only 3 (1/2a, 1/2b, and 4b) of
the 13 serotypes known for this species (11, 22, 32, 33).
Worldwide, most sporadic human cases and most outbreaks have reportedly
been caused by L. monocytogenes serotype 4b (11,
30), including one of the more recent outbreaks in the United
States (9, 10). Most of these epidemic isolates can be
grouped into two closely related homogeneous groups (so-called "epidemic clones") represented by two multilocus enzyme
electrophoresis types and two ribotypes (14, 20, 27, 29,
37). These observations indicate that sensitive strain
discrimination among serotype 4b strains is particularly crucial for
surveillance and monitoring of human listeriosis cases.
The use of several subtyping methods, including multilocus enzyme
electrophoresis, total DNA restriction endonuclease analysis, ribotyping, pulsed-field gel electrophoresis (PFGE), and random amplified polymorphic DNA analysis, for sensitive subtyping of L. monocytogenes has been explored by various groups
(15). Many molecular typing methods offer the advantage of
high discriminating ability and typeability and do not require
specialized reagents such as typing sera and bacteriophages. PFGE using
one or more enzymes is a commonly used and apparently highly
discriminatory molecular subtyping method for L. monocytogenes (15). Major limitations of most
molecular typing methods include a lack of standardization, a need for
highly skilled technical staff, and significant hands-on time required
for performance. Automation may allow laboratories to apply molecular
typing more broadly. The RiboPrinter microbial characterization system
(Qualicon Inc., Wilmington, Del.) is a completely automated subtyping
system based on the principle of ribotyping (16). This
system automates and standardizes all process steps required for
ribotyping, from cell lysis to image analysis, and provides subtyping
results within 8 h. While setup of an automated ribotyping
laboratory requires considerable capital investment, for laboratories
subtyping >1,500 isolates/year, costs on a per-isolate basis may be
lower than for other, more labor-intensive subtyping methods
(39).
Both manual and automated ribotyping methods have been widely used for
subtyping of bacterial isolates (1, 2, 13, 14, 16, 19),
detection and tracking of human and animal listeriosis cases and
outbreaks (9, 36, 38), and tracking of L. monocytogenes contamination patterns in food processing plants
(28). While the restriction enzymes EcoRI and
PvuII have been used most commonly for ribotyping (13,
14), other restriction enzymes have also been used (2,
19). Some previous studies indicated that single-enzyme
ribotyping may be less discriminatory than some other subtyping
methods, particularly for L. monocytogenes serotype 1/2b and
4b strains (4, 35).
To develop improved automated subtyping approaches for L. monocytogenes, we characterized the discriminatory power of
different restriction enzymes for automated ribotyping. We also
specifically explored the use of ribotyping with different restriction
enzymes to improve discrimination of isolates representing the two
epidemic L. monocytogenes serotype 4b clonal groups.
Automated ribotyping.
Ribotyping was performed using the
RiboPrinter microbial characterization system. Briefly, overnight
bacterial cells were picked from brain heart infusion agar plates,
suspended in sample buffer, inactivated by a heat kill step, and
treated with lytic enzymes to release the DNA. The DNA was cut with a
restriction enzyme, and the fragments were electrophoretically
separated and simultaneously transferred to a membrane. A DNA probe for
the Escherichia coli rrnB operon was then hybridized to the
genomic DNA on the membrane. The genetic fingerprint was visualized and captured using a chemiluminescent detection system and a
charge-coupled device camera. Analysis software automatically
characterized and identified the digitalized image.
Characterization consists of combining patterns within a specific
similarity range to form a dynamic ribogroup that reflects the genetic
relatedness of the isolates (6).
To allow the use of restriction enzymes requiring different
time-temperature combinations for optimum performance (Table
1), the RiboPrinter system software has
been modified to allow different digestion times (20 and 120 min) and
temperatures (37 and 60°C). All restriction enzymes were obtained
from New England Biolabs (Cambridge, Mass.).
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TABLE 1.
Digestion time, incubation temperature, and
discriminatory ability of 15 restriction enzymes used for
characterization of 16 L. monocytogenes isolates
|
|
Subtyping results with automated ribotyping using 15 restriction
enzymes.
In an initial screening, 15 restriction enzymes were
tested for their ability to discriminate 16 L. monocytogenes
isolates. These isolates had previously been shown to represent 16 distinct EcoRI ribotypes through the use of manual
ribotyping (7), which allowed for longer gel run times and
better band separation. These initial isolates represented the
EcoRI ribotypes dd 0647, dd 0653, dd 3581, dd 1049, dd 1288, dd 7674, dd 7730, dd 7745, dd 0566, dd 1070, dd 6439, dd 6481, dd 1966, dd 6296, dd 7696, and dd 6323 (7).
Three of the enzymes tested (
BsoBI,
ClaI, and
StyI) consistently produced incomplete digests under the
conditions used. Thus,
patterns were not reproducible and these enzymes
are not recommended
for automated ribotyping of
L. monocytogenes using the digestion
conditions outlined in Table
1.
With the remaining 12 restriction
enzymes, we were able to
differentiate between 1 and 15 different
ribotypes (Table
1). The
suitability of ribotyping for differentiation
of strains was
quantitated using Simpson's index of discrimination
(SID)
(
18). The numerical value of this index indicates the
discriminatory power of a given typing method by estimating the
probability that two unrelated strains are differentiated by this
method. As the numerical index approaches the maximum value of
1 (representing 100% discriminatory ability of a method), the
probability increases that a given method will be able to discriminate
between two unrelated strains. The five restriction enzymes with
the
highest discriminatory ability (SID
0.900) were
PvuII,
EcoRI,
BstEII,
BanI,
and
XhoI (Fig.
1).
PvuII was the most discriminatory
enzyme, yielding 15 different ribotypes. A combination of
PvuII
ribotypes with
ribotypes created by either
XhoI,
BstEII,
AseI,
BanI, or
BglIII allowed
discrimination of all 16 isolates. No
other combination of two
restriction enzymes allowed discrimination
of all 16 isolates. While
this is the first study reporting comparison
of a large number of
restriction enzymes for subtyping of
L. monocytogenes,
our
results are in general agreement with other studies. For example,
Gendel and Ulaszek (
13) showed that
PvuII
ribotyping discriminated
more subtypes among a collection of 72 smoked
salmon isolates
than
EcoRI ribotyping did. In earlier
studies,
EcoRI ribotyping
was shown to be more
discriminatory and suitable for
L. monocytogenes subtyping
than
HindIII or
HaeIII ribotyping (
2,
19).
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FIG. 1.
Ribotypes obtained with enzymes EcoRI,
PvuII, BstEII, BanI, and
XhoI for 16 genotypically distinctive L. monocytogenes isolates. The two isolates with indistinguishable
PvuII ribotypes are marked with asterisks.
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|
Discrimination of epidemic serotype 4b-associated genotypes using
ribotyping with three selected restriction enzymes.
Sensitive
subtyping of L. monocytogenes serotypes 4b and 1/2b is of
particular importance, as these two serotypes form a distinctive subset
(lineage) that is responsible for the majority of human listeriosis
cases (22, 33, 37). Within the lineage containing serotype
1/2b and 4b strains, two distinct clonal groups show particular
prevalence among human listeriosis cases and outbreaks (29,
37). Isolates representing one clonal group have previously been
characterized as ribotype reference pattern DUP-1038 and ribotype dd
0647 (37). This clonal group was linked to human listeriosis outbreaks in France (8), Nova Scotia, Canada
(31), Switzerland (3), and Los Angeles,
Calif. (21). A second clonal group (ribotype reference
pattern DUP-1042, ribotype dd 0653 [37]) has been linked
to human listeriosis outbreaks in Boston (17), Massachusetts (12), and the United Kingdom
(25). Reference patterns DUP-1042 and DUP-1038 each
represent a group of closely related EcoRI ribotypes. These
reference patterns were created by averaging individual closely related
ribotype patterns obtained for multiple isolates. For example, DUP-1042
was previously shown to contain at least two closely related
EcoRI ribotypes (dd 3581 and dd 0653) (7).
We used 71
L. monocytogenes isolates from humans, food, and
other sources, representing the two major serotype 4b epidemic
clones
of
L. monocytogenes, to further evaluate the discriminatory
power of automated ribotyping using different restriction enzymes.
Specifically, 51 and 20 of these isolates had previously been
characterized as the
EcoRI ribotype reference patterns
DUP-1038
and DUP-1042, respectively. From the five restriction enzymes
that allowed the most sensitive discrimination (SID
0.900) in
our initial experiments on 16 diverse isolates, three enzymes
(
PvuII,
EcoRI, and
XhoI) were used to
determine their ability
to differentiate among these isolates.
Restriction enzymes
BanI
and
BstEII were not
included because they produced weak low-molecular-weight
bands, which
often required manual refinement for accurate analysis.
Enzymes
PvuII,
EcoRI, and
XhoI produced more
distinct patterns
amenable to automated analysis and differentiation.
Automated
ribotyping with
PvuII provided the highest
discrimination (SID
= 0.518) (Table
2) among these groups of closely related
isolates.
Combined analysis of ribotype patterns obtained with two
enzymes
allowed a significant increase in discriminatory power, and a
combination of
PvuII and
XhoI data allowed for
the highest discriminatory
ability (Table
2). Forty-four of the 51 DUP-1038 as well as 12
of the 20 DUP-1042 isolates gave identical
patterns with all three
enzymes. Figure
2
shows the ribotype patterns obtained for the
DUP-1038 and DUP-1042
isolates. DUP-1038 and DUP-1042 showed distinct
ribotype patterns, and
careful examination of
EcoRI ribotype patterns
allowed
differentiation of four different ribotypes among DUP-1042
isolates and
three different ribotypes among DUP-1038 isolates.
The three DUP-1038
ribotypes differed by the presence or absence
of weak bands in the 8- to 10-kb range, while the four DUP-1042
isolates differed by the
presence or absence of weak bands in
the 10- to 13-kb range.
PvuII ribotype patterns, on the other
hand, generally
showed much more distinct differences in banding
patterns.
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TABLE 2.
Subtype discrimination among epidemic clones DUP-1038
(n = 51) and DUP-1042 (n = 20) by
ribotyping with different restriction enzymes
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FIG. 2.
Ribotype patterns obtained with enzymes
EcoRI, PvuII, and XhoI among all
DUP-1038 and DUP-1042 isolates included in this study. The number of
isolates within each ribotype (separated by DUP-1038 and DUP-1042
isolates) is indicated on the left.
|
|
Although considered a highly discriminatory subtyping method for
L. monocytogenes (
15), even PFGE with three
different restriction
enzymes often appears not to discriminate within
these clonal
groups, including among isolates from temporally and/or
geographically
distinct outbreaks. For example, isolates from the 1983 listeriosis
outbreak in Massachusetts and isolates from the 1987-1989
outbreak
in England were indistinguishable by PFGE using the
restriction
enzymes
AscI,
ApaI, and
SmaI. Similarly, the same enzymes could
not differentiate
isolates from the outbreak in Los Angeles in
1985 and from the outbreak
in Vaud, Switzerland, from 1983 to
1987 (
5). Our results
are thus consistent with previous results,
which show the highly clonal
nature of the serotype 4b clonal
groups (
5,
29). Sensitive
subtyping of these isolates represents
a significant challenge and may
require novel, possibly genomics-based,
approaches.
Conclusions.
Our results show that hierarchical ribotyping
using different enzymes allows improved discrimination of L. monocytogenes isolates, including strains in the epidemic serotype
4b clonal groups. While surveillance and epidemiological investigations
of human listeriosis cases may profit considerably from subtyping using
multiple enzymes and automated ribotyping, currently more
labor-intensive and possibly less standardized additional typing
methods may be necessary to further discriminate strains in these
clonal groups.
| |
ACKNOWLEDGMENTS |
Some of the material described in this paper is based upon work
supported by the USDA National Research Initiative under award no.
99-35201-8074 to M. Wiedmann.
We thank Elizabeth Mangiaterra of Qualicon Inc. for technical assistance.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Food Science, 412 Stocking Hall, Cornell University, Ithaca, NY 14853. Phone: (607) 254-2838. Fax: (607) 254-4868. E-mail:
mw16{at}cornell.edu.
| |
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Journal of Clinical Microbiology, August 2001, p. 3002-3005, Vol. 39, No. 8
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.8.3002-3005.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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