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Journal of Clinical Microbiology, July 1999, p. 2176-2182, Vol. 37, No. 7
Laboratory of Enteric Pathogens,
Received 2 November 1998/Returned for modification 14 January
1999/Accepted 23 March 1999
In the 1990s, Salmonella enterica subsp.
enterica serovar Enteritidis has caused 15 outbreaks in
Finland; 12 of them were caused by phage type 1 (PT1) and PT4. Thus
far, there has been no clear evidence as to the source of these
Salmonella Enteritidis PT1 and PT4 strains, so it was
necessary to try to characterize them further. Salmonella
Enteritidis PT1 (n = 57) and PT4 (n = 43) isolates from different sources were analyzed by genomic
pulsed-field gel electrophoresis (PFGE), plasmid profiling, and
antimicrobial resistance testing to investigate the distribution of
their subtypes in Finland. It was also hoped that this investigation
would help in identifying the sources of the infections, especially the
sources of the outbreaks caused by PT1 and PT4 in the 1990s. The
results showed that both PFGE and plasmid profiling, but not
antimicrobial susceptibility testing, were capable of differentiating
isolates of Salmonella Enteritidis PT1 and PT4. By
genotypic methods, it was possible to divide both PT1 and PT4 isolates
into 12 subtypes. It could also be shown that all PT1 outbreak isolates
were identical and, at least with this collection of isolates, that the
outbreaks did not originate from the Baltic countries or from Russia,
where this phage type predominates. It was also established that the outbreaks caused by PT4 all had different origins. Valuable information for future investigations was gained on the distribution of molecular subtypes of strains that originated from the tourist resorts that are
popular among Finns and of strains that were isolated from livestock.
Salmonella enterica
subsp. enterica serovar Enteritidis is the most common
serovar that causes salmonellosis in humans. Since the 1980s, there has
been a dramatic increase in the number of reported findings of this
serovar in Europe and worldwide (8, 13, 19). The most
frequent reservoir for Salmonella Enteritidis has been
poultry, especially eggs (19). The occurrence of the phage
types of Salmonella Enteritidis in different geographical areas has varied: phage type 1 (PT1) has been common in the Baltic countries and Russia (7), whereas PT4 most often has been
seen in Western European countries (9, 20). PT8 apparently
has been a frequent finding in the United States (8).
The proportion of Salmonella Enteritidis causing
indigenously acquired salmonellosis has greatly increased in Finland in
the past few years. The strains that have been the cause of this
increase have originated from abroad, whereas the proportion of
domestic strains has remained fairly constant (Fig.
1). Salmonella
Enteritidis has caused 15 domestic outbreaks during the 1990s; 9, 3, and 3 were caused by Salmonella Enteritidis PT1,
Salmonella Enteritidis PT4, and other phage types,
respectively (21a).
When one is tracing the origin of a salmonella infection, it is
important to differentiate between strains in great detail. Traditional
epidemiological methods include biotyping, serotyping, and phage typing
of isolates, as well as antimicrobial susceptibility testing, although
these methods do not always give enough information for epidemiological
purposes. Also, phage typing is not available in all laboratories, and
certain strains of Salmonella Enteritidis can change phage
types (1, 16, 17, 27, 28). Some phage types may
predominate in a geographical area, a fact which may limit the
use of phage typing in investigating local outbreaks. However, more
information can be gathered by analyzing plasmids from the isolates
(2, 29) or chromosomal DNA by different molecular
techniques, such as ribotyping (6), IS200 typing (23), or pulsed-field gel electrophoresis (PFGE)
(15).
In Finland, data on the epidemiologic characteristics and potential
reservoirs of Salmonella Enteritidis PT1 and PT4 have been
insufficient. To gain more detailed information, the highly discriminatory technique PFGE was chosen for subtyping of the strains
of these phage types (11, 14, 18). Plasmid analysis and
antimicrobial susceptibility testing were used to complement the
results of PFGE.
Salmonella isolates.
All strains had
previously been phage typed as Salmonella Enteritidis PT1
and PT4 according to the scheme of Ward et al. (31) at the
Laboratory of Enteric Pathogens and stored at Salmonella Enteritidis PT1.
Fifty-seven strains
of Salmonella Enteritidis PT1 were studied (Table
1); 26 of the 51 human
isolates were of domestic origin, and 6 of them represented the PT1
outbreaks in a 5-year period from 1991 to 1995 (Fig.
2 and Table
2). Two isolates (chicken liver and
eggshell) were obtained from the poultry farm that was the source of
the outbreaks in Turku, Finland (10). Twenty-five strains
were of foreign origin; 4 of them were obtained from the Baltic
countries (kindly sent by Unna Jöks, Central Laboratory of
Microbiology, Health Protection Inspectorate, Tallinn, Estonia), and 21 were isolated from Finnish tourists who had been abroad preceding their
salmonella infections. These nonoutbreak strains were selected randomly
to represent strains from various countries. Three nonoutbreak strains
were from animals, and one was from foodstuffs.
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Copyright © 1999, American Society for Microbiology. All rights reserved.
Salmonella Enteritidis Phage Types 1 and 4: Pheno- and
Genotypic Epidemiology of Recent Outbreaks in Finland
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
View larger version (19K):
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FIG. 1.
Number of all salmonella infections, number of domestic
and foreign Salmonella (S.) Enteritidis infections in
Finland between 1965 and 1997 (21a), and number of Finnish
passengers on charter flights (statistics of the Civil Aviation
Administration and Statistics Finland).
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
70°C in sterilized
skim milk or at room temperature in nutrient agar tubes. Along with a
set of PT1 and PT4 outbreak isolates, representative sets of
nonoutbreak isolates from humans, as well as all available PT1 and PT4
isolates from livestock and foodstuffs, were included in the study.
TABLE 1.
Salmonella Enteritidis PT1 isolates
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FIG. 2.
Geographic occurrence of Salmonella
Enteritidis PT1 ( 
) and PT4 (
) outbreaks in Finland in the 1990s.
See Table 2 for the number of infections in each outbreak.
TABLE 2.
Number of infections in outbreaks
Salmonella Enteritidis PT4.
Forty-three
Salmonella Enteritidis PT4 strains were studied (Table
3); 14 of
the 32 human isolates were of domestic origin, and 6 of them
represented three PT4 outbreaks between 1993 and 1995. Domestic
nonoutbreak isolates from 1993 to 1995 were not available, but eight
isolates from 1997 to 1998 were included in this study. Eighteen
nonoutbreak strains of foreign origin, isolated in Finland from Finnish
tourists who had been abroad preceding their salmonella infections,
were selected randomly to represent strains from various countries.
Eleven strains were from animals.
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PFGE. Salmonella strains were grown overnight on Drigalski-Conradi agar plates at 37°C. Bacterial cells were suspended in 1,200 µl of TEN (0.1 M Tris-HCl, 0.15 M NaCl, 0.1 M EDTA [pH 7.5]) to an optical density at 600 nm of 0.150 to 0.200. This cell suspension was mixed in equal parts with molten 2% low-melting-point agarose (SeaPlaque agarose; FMC BioProducts, Rockland, Maine), and the mixture was pipetted into plug molds. The plugs were incubated overnight at 55 to 57°C in ES buffer (0.5 M EDTA, 1% N-(auroylsarcosine) with 0.15 mg of proteinase K per ml. The plugs were washed with TE buffer (10 mM Tris-HCl, 1 mM EDTA [pH 8.0]) for 30 min, with TE buffer-4 mM phenylmethylsulfonyl fluoride for 30 min to inactivate proteinase K, and with TE buffer three times for 30 min each time. The conditions for restriction endonuclease digestion and PFGE were essentially those described by Thong et al. (26). Chromosomal DNA was digested with 10 U of restriction enzymes XbaI, SpeI, and NotI (Boehringer Mannheim GmbH, Mannheim, Germany) overnight at 37°C. Electrophoresis was performed at 210 V on 1.0% SeaKem ME agarose gels (FMC BioProducts) with a Gene Navigator system (Pharmacia, Uppsala, Sweden) or with CHEF Mapper systems (Bio-Rad Laboratories, Richmond, Calif.). Running conditions were as follows: XbaI digests, 5 to 70 s for 24 h; SpeI digests, 5 to 40 s for 24 h; and NotI digests, 1 to 20 s for 20 h. A bacteriophage lambda ladder consisting of concatemers in increments of 48.5 kbp (New England BioLabs Inc., Beverly, Mass.) was used as a molecular weight standard. Any difference between two profiles was considered sufficient to distinguish two different PFGE profiles. XbaI-digested PFGE profiles were named with uppercase letters starting at A; the numbers 1 and 4 indicate whether the strain belonged to PT1 or PT4, respectively.
Plasmid profiling. Plasmid DNA was isolated by the alkaline lysis method as described earlier (5). Samples were analyzed by electrophoresis at 120 V for 70 min on horizontal 0.9% SeaKem ME agarose gels with a CIBCO BRL Horizon 20.25 system (Life Technologies Inc., Gathersburg, Md.). The gels were stained for 30 min with ethidium bromide (0.5 µg/ml) and photographed under UV illumination. Plasmid-containing strains RH 4240 (39R861 [30]) and RH 4241 (V517 [12]) were used as controls. Plasmid profiles were named with lowercase letters starting at a.
Antimicrobial susceptibility testing. The antimicrobial susceptibilities of the strains were determined by the agar diffusion method on semisynthetic Iso-Sensitest medium with the following antimicrobial agents (4): ampicillin, chloramphenicol, ceftriaxone, imipenem, mecillinam, nalidixic acid, neomycin, sulfonamide, tetracycline, trimethoprim, streptomycin, and ciprofloxacin (Neo-Sensitabs; A/S Rosco, Taastrup, Denmark). Inhibition zones were interpreted according to the recommendations of the Swedish Reference Group for Antibiotics (24).
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Salmonella Enteritidis PT1. Seven banding patterns (subtypes 1A to 1G) were observed among the 57 PT1 strains studied by PFGE (Table 1 and Fig. 3) when chromosomal DNAs of the strains were digested with restriction enzyme XbaI. Different test conditions showed that subtypes 1B, 1E, and 1F had fragments at 676 and 661 kb, although only one of these was visible in the fragment pattern (Fig. 3). All eight outbreak strains from Turku and Vieremä, in addition to three nonoutbreak strains belonged to PFGE subtype 1F (Table 1). Among the nonoutbreak strains, the most common PFGE subtypes were 1A (20 strains) and 1B (22 strains), whereas subtypes 1C, 1D, and 1E each included only one strain.
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one each from Turku and Vieremä, one from
chicken liver, two from the Baltic countries, and one from
Finnish cattlewere also digested with restriction enzymes
SpeI and NotI. All six
SpeI-digested strains had indistinguishable PFGE profiles. When digested with NotI, strains from Turku, Vieremä,
and chicken liver had similar PFGE profiles, but they were different
from those of the two strains from the Baltic countries and the single strain from Finnish cattle (data not shown).
Seven plasmid profiles (a to g) were identified by plasmid analysis
(Table 1 and Fig. 4). Profile a had one
plasmid; b had four plasmids; c had three; d, e, and f each had two;
and g was plasmid free (Fig. 4). Forty-seven of the 57 strains studied, including all 8 outbreak strains, had plasmid profile a, regardless of
the origin (human or nonhuman, domestic or foreign) (Table 1).
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Salmonella Enteritidis PT4. Seven banding patterns (subtypes 4A to 4G) were represented among the 43 PT4 strains studied by PFGE after XbaI restriction of genomic DNAs (Table 3 and Fig. 5). With different test conditions, it could be seen that subtypes 4A, 4B, 4C, 4F, and 4G had fragments at 646 and 661 kb, although only one of these was visible in the fragment pattern (Fig. 5). Of the 43 strains studied, 33, including the outbreak strains from Leppävirta, belonged to PFGE subtype 4A (Table 3).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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A large set of Salmonella Enteritidis PT1 and PT4 isolates from different sources was analyzed by PFGE, plasmid profiling, and antimicrobial resistance testing to gain knowledge of the distribution of their potential subtypes in Finland. It was especially hoped that these analyses would help in determining the sources of the several outbreaks caused by PT1 and PT4 isolates in the 1990s.
Finland has traditionally had very strict salmonella control for livestock, a fact which has made it easier to keep indigenously acquired salmonella infections rare, unlike in many other European countries. The European Union allowed Finland to continue with this control system even after it joined the Union. Most of the salmonella infections diagnosed in Finland have been related to a trip abroad (21, 22). In the mid-1980s, infections caused by Salmonella Enteritidis began to increase in parallel with the increasing number of Finns vacationing abroad (Fig. 1). In the 1990s, Salmonella Enteritidis caused 15 outbreaks in Finland; 12 of them were caused by PT1 and PT4. However, it remained unclear from where these outbreaks originated; it was possible that the infections were connected to imported foodstuffs, that they were secondary infections caused by strains of foreign origin, or that there were some hidden reservoirs in Finnish production animals. Thus, it was necessary to try to characterize the PT1 and PT4 isolates further.
Salmonella Enteritidis PT1 was the cause of eight outbreaks in the area around Turku over a period of 5 years. In 1995, the infection source was finally found to be a poultry farm near Turku. This was the first time that Salmonella Enteritidis PT1 was detected in a Finnish commercial layer flock (10). As a result, the poultry farm was closed down, but the original source of the PT1 strain was never discovered. There were some suspicions that this strain was somehow imported from the Baltic countries, where Salmonella Enteritidis PT1 strains have been the most common Salmonella strains found in eggs (7).
The results of this study confirmed the earlier findings (10) that the Salmonella Enteritidis PT1 1Fa strain that had caused the outbreaks in Turku indeed had originated from the nearby poultry farm. It was interesting that the strains isolated in Estonia and those isolated from the Finnish tourists who had visited the Baltic countries were of type 1Aa, thus differing from the 1Fa outbreak strain and suggesting that the original source was not the Baltic countries. The 1Fa strain was also found to be the cause of the outbreak in Vieremä, which is located about 500 km northeast of Turku. Unfortunately, no connection between the outbreaks caused by identical strains in Vieremä and Turku could be found either at the time of the outbreaks or later on. Subtype 1Fa seemed to be very rare in Finland: only 1 of the 48 nonoutbreak strains belonged to this subtype, which differed from the other nonoutbreak strain subtypes by four to nine chromosomal fragments.
Among the nonoutbreak PT1 strains, subtype 1Aa seemed to be associated with Eastern Europe, and subtype 1Ba seemed to be associated with Western Europe. Type 1Ba also included two isolates from Finnish cattle. This was an important finding because there has been no identified reservoir for Salmonella Enteritidis PT1 in Finland since the commercial layer flock outbreaks in 1991 to 1995.
Salmonella Enteritidis PT4 has caused three outbreaks in different parts of Finland in the 1990s: the first was in Leppävirta in April 1993, the second was in Rauma in March 1995, and the third was in Kotka in December 1995. No connections were found between these three outbreaks at the time, and their sources were never established.
Salmonella Enteritidis PT4 is the most common phage type that contaminates eggs in Central Europe (20) and in England (9). In Finland, however, Salmonella Enteritidis PT4 has been found very rarely in cattle, less than 10 times in turkeys, and never in eggs. Imported meat has occasionally tested positive for Salmonella Enteritidis PT4.
Most of the PT4 strains belonged to PFGE subtype 4A. However, plasmid profiling was able to distinguish six profiles within this PFGE subtype. Among the 33 subtype 4A strains, only the outbreak strain in Leppävirta belonged to subtype 4Aa. Subtype 4Eb, which caused the outbreak in Rauma, differed from subtype 4Aa by three PFGE and plasmid fragments and was not found in other strains investigated here. The outbreak strain isolated in Kotka belonged to subtype 4Bg, which differed from subtype 4Ab only by one plasmid (about 45 to 60 kb), which was about the same size as the fragment that distinguished subtypes 4B and 4A in PFGE. Thus, strains of subtypes 4Bg and 4Ab could be of the same origin if these strains had lost or acquired a plasmid of this size. This finding suggests that subtypes 4Bg and 4Ab isolated from Finnish cows potentially have a reservoir in Finnish cattle and that this reservoir might have been the source of the outbreak in Kotka if these strains had lost or acquired a plasmid. These suggestions would also explain the 1997 and 1998 human isolates that belonged to subtype 4Ab. In addition, 4Bg and 4Eb differed by four PFGE fragments, whereas 4Bg and 4Aa differed by only one PFGE fragment. This one fragment was also smaller than 125 kb, a result which could indicate interference from an unstable fragment of plasmid DNA (14). However, these two subtypes, 4Bg and 4Aa, differed by four plasmids. Considering all of these results, it seems that the outbreaks in Leppävirta, Rauma, and Kotka had different origins.
This study showed that both PFGE and plasmid profiling were capable of differentiating between Salmonella Enteritidis PT1 and PT4 isolates. Some of the isolates with different PFGE subtypes had a difference of only one or two fragments in their PFGE banding patterns when digested with XbaI. Recent point mutations within a subtype might account for these minor differences (25), although the study of Murase et al. (13) concluded that the PFGE profiles of strains digested with XbaI were not affected by point mutations. Salmonellae can spontaneously lose or acquire plasmids (3), a fact which limits the use of plasmid analysis for epidemiological investigations. In this study, however, if there was a difference of several fragments in the plasmid profiles of two strains, it was considered to support the results of PFGE showing fragment patterns that differed by only a few fragments. Additional tests were done with two other restriction enzymes, SpeI and NotI. The discriminatory power of these two enzymes was, however, lower than that of XbaI.
It is also worth mentioning that without phage typing, PFGE would not have been effective in distinguishing between PT1 and PT4, since some strains showed almost identical PFGE banding patterns (1F and 4G; 1B and 4A), regardless of their phage type. In addition, antimicrobial susceptibility testing was not useful because most of the strains were sensitive to all antimicrobial agents tested.
With this collection of isolates, the genotypic methods used here showed that all PT1 isolates associated with the outbreaks were identical to each other and differed from those associated with the Baltic countries and Russia, where this phage type predominates (7). It was also established that the outbreaks caused by PT4 all had different origins. Furthermore, valuable information for future investigations was gained on the distributions of the molecular subtypes of strains that originated from the tourist resorts that are popular among Finns and of the subtypes of strains isolated from domestic production animals.
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ACKNOWLEDGMENTS |
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We are grateful to Unna Jöks for providing strains from the Baltic countries. We also thank Liisa Immonen, Tarja Heiskanen, and Ritva Taipalinen for skillful technical assistance and advice, Sinikka Pelkonen and Saija Hallanvuo for helpful discussions and useful comments, and Maarit Koukkari for editorial assistance.
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FOOTNOTES |
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* Corresponding author. Mailing address: National Public Health Institute, Laboratory of Enteric Pathogens, Mannerheimintie 166, FIN-00300 Helsinki, Finland. Phone: 358-9-47448245. Fax: 358-9-47448238. E-mail: anja.siitonen{at}ktl.fi.
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REFERENCES |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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| 1. | Brown, D. J., D. L. Baggesen, D. J. Platt, and J. E. Olsen. 1999. Phage type conversion in Salmonella enterica serotype Enteritidis caused by the introduction of a resistance plasmid of incompatibility group X (IncX). Epidemiol. Infect. 122:19-22[Medline]. |
| 2. | Brown, D. J., E. J. Threlfall, M. D. Hampton, and B. Rowe. 1993. Molecular characterization of plasmids in Salmonella enteritidis phage types. Epidemiol. Infect. 110:209-216[Medline]. |
| 3. | Brown, D. J., E. J. Threlfall, and B. Rowe. 1991. Instability of multiple drug resistance plasmids in Salmonella typhimurium isolated from poultry. Epidemiol. Infect. 106:247-257[Medline]. |
| 4. | Casals, J. B., and N. Pringler. 1991. Antibacterial and antifungal sensitivity testing using Neo-Sensitabs, 9th ed. A/S Rosco Diagnostica, Taastrup, Denmark. |
| 5. | Grinsted, J., and P. M. Bennet. 1988. Preparation and electrophoresis of plasmid DNA. Methods Microbiol. 21:129-142. |
| 6. | Gruner, E., L. G. Martinetti, R. K. Hoop, and M. Altwegg. 1994. Molecular epidemiology of Salmonella enteritidis. Eur. J. Epidemiol. 10:85-89[Medline]. |
| 7. | Hasenson, L. B., L. Kaftyreva, V. G. Laszló, E. Woitenkova, and M. Nesterova. 1992. Epidemiological and microbiological data on Salmonella enteritidis. Acta Microbiol. Hung. 39:31-39[Medline]. |
| 8. |
Hickman-Brenner, F. W.,
A. D. Stubbs, and J. J. Farmer, III.
1991.
Phage typing of Salmonella enteritidis in the United States.
J. Clin. Microbiol.
29:2817-2823 |
| 9. | Humphrey, T. J., A. Baskerville, S. Maver, B. Rove, and S. Hopper. 1989. Salmonella enteritidis phage type 4 from the contents of intact eggs: a study involving naturally infected hens. Epidemiol. Infect. 103:415-423[Medline]. |
| 10. | Johansson, T. M.-L., R. Schildt, S. Ali-Yrkkö, A. Siitonen, and R. L. Maijala. 1996. The first Salmonella Enteritidis phage type 1 infection of a commercial layer flock in Finland. Acta Vet. Scand. 37:471-480[Medline]. |
| 11. |
Liebisch, B., and S. Schwarz.
1996.
Molecular typing of Salmonella enterica subsp. enterica serovar Enteritidis isolates.
J. Med. Microbiol.
44:52-59 |
| 12. | Macrina, F. L., D. J. Kopecko, K. R. Jones, D. J. Ayers, and S. M. McCowen. 1978. A multiple plasmid-containing Escherichia coli strain: convenient source of size reference plasmid molecules. Plasmid 1:417-420[Medline]. |
| 13. | Murase, T., T. Okitsu, A. Nakamura, A. Matsushima, and S. Yamai. 1996. An epidemiological study of Salmonella enteritidis by pulsed-field gel electrophoresis (PFGE): several PFGE patterns observed in isolates from a food poisoning outbreak. Microbiol. Immunol. 40:873-875[Medline]. |
| 14. |
Olsen, J. E.,
M. N. Skov,
E. J. Threlfall, and D. J. Brown.
1994.
Clonal lines of Salmonella enterica serotype Enteritidis documented by IS200-, ribo-, pulsed-field gel electrophoresis and RFLP typing.
J. Med. Microbiol.
40:15-20 |
| 15. | Powell, N. G., E. J. Threlfall, H. Chart, and B. Rowe. 1994. Subdivision of Salmonella enteritidis PT 4 by pulsed-field gel electrophoresis: potential for epidemiological surveillance. FEMS Microbiol. Lett. 119:193-198[Medline]. |
| 16. | Powell, N. G., E. J. Threlfall, H. Chart, S. L. Schofield, and B. Rowe. 1995. Correlation of change in phage type with pulsed field profile and 16S rrn profile in Salmonella enteritidis phage types 4, 7 and 9a. Epidemiol. Infect. 114:403-411[Medline]. |
| 17. | Rankin, S., and D. J. Platt. 1995. Phage conversion in Salmonella enterica serotype Enteritidis: implications for epidemiology. Epidemiol. Infect. 114:227-236[Medline]. |
| 18. |
Ridley, A. M.,
E. J. Threlfall, and B. Rowe.
1998.
Genotypic characterization of Salmonella enteritidis phage types by plasmid analysis, ribotyping, and pulsed-field gel electrophoresis.
J. Clin. Microbiol.
36:2314-2321 |
| 19. | Rodrigue, D. C., R. V. Tauxe, and B. Rowe. 1990. International increase in Salmonella enteritidis: a new pandemic? Epidemiol. Infect. 105:21-27[Medline]. |
| 20. | Schroeter, A., L. R. Ward, B. Rowe, D. Protz, M. Hartung, and R. Helmuth. 1994. Salmonella enteritidis phage types in Germany. Eur. J. Epidemiol. 10:645-648[Medline]. |
| 21. | Siitonen, A. 1998. Human salmonelloses in Finland, p. 254-257. In 4th World Congress on Foodborne Infections and Intoxications. |
| 21a. | Siitonen, A. 1998. Statistics of the Laboratory of Enteric Pathogens National Public Health Institute, Helsinki, Finland. Unpublished data. |
| 22. | Siitonen, A., and R. Puohiniemi. 1997. Epidemiology of human salmonelloses in Finland: findings of domestic and foreign origins. In Program and abstracts of the 37th Interscience Conference on Antimicrobial Agents and Chemotherapy. |
| 23. | Stanley, J., C. S. Jones, and E. J. Threlfall. 1991. Evolutionary lines among Salmonella enteritidis phage types are identified by insertion sequence IS200 distribution. FEMS Microbiol. Lett. 82:83-90. |
| 24. |
Swedish Reference Group for Antibiotics.
1990.
Antimicrobial susceptibility testing of bacteriaa reference and a methodology manual.
The Swedish Medical Society and Statens Bakteriologiska Laboratorium, Stockholm, Sweden.
|
| 25. | Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33:2233-2239[Medline]. |
| 26. |
Thong, K.-L.,
Y.-M. Cheong,
S. Puthucheary,
C.-L. Koh, and T. Pang.
1994.
Epidemiologic analysis of sporadic Salmonella typhi isolates and those from outbreaks by pulsed-field gel electrophoresis.
J. Clin. Microbiol.
32:1135-1141 |
| 27. | Threlfall, E. J., and H. Chart. 1993. Interrelationship between strains of Salmonella enteritidis. Epidemiol. Infect. 111:1-8[Medline]. |
| 28. | Threlfall, E. J., H. Chart, L. R. Ward, J. D. H. de Sa, and B. Rowe. 1993. Interrelationships between strains of Salmonella enteritidis belonging to phage types 4, 7, 7a, 8, 13, 13a, 23, 24 and 30. J. Appl. Bacteriol. 75:43-48[Medline]. |
| 29. | Threlfall, E. J., M. D. Hampton, H. Chart, and B. Rowe. 1994. Use of plasmid profile typing for surveillance of Salmonella enteritidis phage type 4 from humans, poultry and eggs. Epidemiol. Infect. 112:25-31[Medline]. |
| 30. | Threlfall, E. J., B. Rowe, J. L. Ferguson, and L. R. Ward. 1986. Characterization of plasmids conferring resistance to gentamicin and apramycin in strains of Salmonella typhimurium phage type 204c isolated in Britain. J. Hyg. 97:419-426. |
| 31. | Ward, L. R., J. D. H. de Sa, and B. Rowe. 1987. A phage-typing scheme for Salmonella enteritidis. Epidemiol. Infect. 99:291-294[Medline]. |
Journal of Clinical Microbiology, July 1999, p. 2176-2182, Vol. 37, No. 7
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Copyright © 1999, American Society for Microbiology. All rights reserved.
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JANTUNEN, M. E., SAXEN, H., LUKINMAA, S., ALA-HOUHALA, M., SIITONEN, A.
(2001). Genomic identity of pyelonephritogenic Escherichia coli isolated from blood, urine and faeces of children with urosepsis. J Med Microbiol
50: 650-652
[Abstract] [Full Text] -
Liebana, E., Garcia-Migura, L., Breslin, M. F., Davies, R. H., Woodward, M. J.
(2001). Diversity of Strains of Salmonella enterica Serotype Enteritidis from English Poultry Farms Assessed by Multiple Genetic Fingerprinting. J. Clin. Microbiol.
39: 154-161
[Abstract] [Full Text] -
Desai, M., Threlfall, E. J., Stanley, J.
(2001). Fluorescent Amplified-Fragment Length Polymorphism Subtyping of the Salmonella enterica Serovar Enteritidis Phage Type 4 Clone Complex. J. Clin. Microbiol.
39: 201-206
[Abstract] [Full Text]
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