Outbreak of food poisoning caused by lunch boxes prepared by a company contaminated with multidrug resistant Salmonella typhimurium DT104.
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ABSTRACT: Strains of salmonella that are resistant to antimicrobial agents have become a worldwide health problem. A distinct strain of Salmonella enterica serotype typhimurium, known as definitive type 104 (DT104), is resistant to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline and has become a major cause of illness in humans and animals in Europe, especially the United Kingdom. To characterize typhimurium DT104 infections in the United States, we analyzed data collected by local and state health departments and public health laboratories between 1979 and 1996 in national surveys of the antimicrobial-drug resistance of salmonella. Selected typhimurium isolates with the five-drug pattern of resistance were phage typed. The prevalence of typhimurium isolates with the five-drug pattern of resistance increased from 0.6 percent in 1979-1980 to 34 percent in 1996. In 1994-1995, such isolates were identified in samples from 36 of the 46 surveillance sites (78 percent). Thirty-nine of 43 typhimurium isolates with the five-drug pattern of resistance identified in 1994-1995 and 1996 were phage type DT104 or a closely related phage type. Multidrug-resistant typhimurium DT104 has become a widespread pathogen in the United States. More prudent use of antimicrobial agents in farm animals and more effective disease prevention on farms are necessary to reduce the dissemination of multidrug-resistant typhimurium DT104 and to slow the emergence of resistance to additional agents in this and other strains of salmonella.New England Journal of Medicine 06/1998; 338(19):1333-8. · 51.66 Impact Factor
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ABSTRACT: Between 1 August and 15 September 2000, 361 cases of Salmonella enterica serotype Typhimurium definitive phage type (DT) 104, resistant to ampicillin, chloramphenicol, streptomycin, sulphonamides, spectinomycin and tetracycline (R-type ACSSuSpT), were identified in England and Wales residents. Molecular typing of 258 isolates of S. Typhimurium DT104 R-type ACSSuSpT showed that, although isolates were indistinguishable by pulsed-field gel electrophoresis, 67% (174/258) were characterized by a particular plasmid profile. A statistically significant association between illness and consumption of lettuce away from home was demonstrated (OR = 7.28; 95% CI=2.25-23.57; P=0.0006) in an unmatched case-control study. Environmental investigations revealed that a number of food outlets implicated in the outbreak had common suppliers of salad vegetables. No implicated foods were available for microbiological testing. An environmental audit of three farms that might have supplied salad vegetables to the implicated outlets did not reveal any unsafe agricultural practices. The complexity of the food supply chain and the lack of identifying markers on salad stuffs made tracking salad vegetables back to their origin extremely difficult in most instances. This has implications for public health since food hazard warnings and product withdrawal are contingent on accurate identification of the suspect product.Epidemiology and Infection 05/2003; 130(2):169-78. · 2.87 Impact Factor
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ABSTRACT: A total of 674 Salmonella serovar Typhimurium (S. Typhimurium) strains consisting of 522 domestic strains and 152 imported strains isolated in Tokyo, 1980-1998, were examined regarding their drug-resistance and phage-type. Domestic strains accounted for 6.2% of all Salmonella (8,359 strains) isolated from domestic cases, and imported strains accounted for 3.7% of all Salmonella (4,083 strains) isolated from imported cases. A drug-resistance test using 9 drugs (CP, TC, SM, KM, ABPC, ST, NA, FOM, and NFLX) showed that 245 strains (46.9%) of the domestic strains and 109 strains (71.7%) of the imported strains were resistant to some of the drugs, excluding FOM and NFLX. Drugs with a high resistance rate were TC, SM, ABPC, and CP for both groups. Drug-resistance patterns of the resistant strains varied among the 40 types. Among those, prevalent patterns recognized were CP.TC.SM.ABPC, CP.TC.SM.KM.ABPC, TC.SM, SM, and TC.KM in the domestic strains, and TC, CP.TC.SM.ABPC, CP.TC.SM.KM.ABPC, CP.TC.SM.KM.ABPC.ST and TC.KM in the imported strains. The results of the phage-typing test revealed that 31 strains of 52 domestic strains tested, and 13 strains of 46 imported strains tested were definitive type 104 (DT104). Those resistance patterns were CP.TC.SM.ABPC.SU (43 strains) and CP.TC.SM.KM.ABPC.SU (1 strain).Kansenshogaku zasshi. The Journal of the Japanese Association for Infectious Diseases 12/1999; 73(11):1087-94.
Jpn. J. Infect. Dis., 58, 2005
Laboratory and Epidemiology Communications
Outbreak of Food Poisoning Caused by Lunch Boxes Prepared by a Company
Contaminated with Multidrug Resistant Salmonella Typhimurium DT104
Masumi Taguchi*, Kazuko Seto, Masashi Kanki, Teizo Tsukamoto,
Hidemasa Izumiya1 and Haruo Watanabe1
Osaka Prefectural Institute of Public Health, Osaka 537-0025 and
1National Institute of Infectious Diseases, Tokyo 162-8640
Communicated by Haruo Watanabe
(Accepted January 19, 2005)
*Corresponding author: Mailing address: Osaka Prefectural Insti-
tute of Public Health, 1-3-69 Nakamichi, Higashinari-ku, Osaka
537-0025, Japan. Tel: +81-6-6972-1321, Fax: +81-6-6972-0772,
Salmonella enterica serovar Typhimurium definitive phage
type (DT) 104 was first isolated in the United Kingdom in
1984. It was isolated widely from men and animals in
Europe and the United States in the 1990s (1-3). Though it
was first isolated in Japan in 1987 (4), prior to 2003 there
were relatively few cases of food poisoning by the organism,
and no large-scale food poisoning outbreak such as that caused
by S. Enteritidis (5). However, in September 2003, a large-
scale outbreak of food poisoning by S. Typhimurium broke
out in Osaka through the distribution of cooked food.
On September 4, a local public health bureau in Kyoto
Prefecture received a report that many employees of an
institution were absent due to abdominal pain, diarrhea, and
fever. It was found that they had consumed lunch boxes
distributed by a cooked food-provider (Company A) in Osaka.
On September 9, a medical facility in Osaka Prefecture
reported to the local health bureau on food poisoning cases
in a kindergarten. The patients exhibited abdominal pain,
vomiting, and diarrhea. They also had consumed lunch boxes
supplied by the same Company A, which daily distributed
18,681 lunch boxes to 3,081 institutions and 1,100 lunch boxes
to 28 kindergartens. The September outbreak affected 144
institutional workers and 214 kindergarteners. The chief
symptoms were diarrhea (355 patients, or 99% of the total),
abdominal pain (292 patients, 83%) and fever (256 patients,
72%). The distribution of the cases indicated that lunch boxes
prepared by Company A on September 1 and 4, respectively,
caused the outbreaks in the institutions and kindergartens.
S. Typhimurium was isolated from 77 of the 91 patients
from whom stool samples were taken. However, 46 cooked
food specimens for institutions prepared in August 27-
September 2 and 40 specimens for kindergartens prepared in
September 1–5 that were retained according to the Japanese
food regulatory rule were negative for the organism. Ten swab
specimens from the facilities of Company A were also nega-
tive. The responsible food material could not be identified by
analysis of the consumption pattern. Investigation of the food
processing facilities indicated that the cause of the outbreak
may have been insufficient sterilization of machines, such as
dishwashers or vacuum coolers. The difficulty of detecting
the causative bacteria from the food materials in the present
case may have been due to the low-level or uneven distribu-
tion of the contamination, as suggested by the low incidence
of affected individuals, i.e., only 358 patients among nearly
A total of 49 isolates, 8 from the affected institutions (5
isolated by the Osaka Prefectural Institute of Public Health
and 3 by the Kyoto Prefectural Institute of Hygienic and
Environmental Sciences) and 41 isolates from kindergartens
(all isolated by the Osaka City Institute of Public Health and
Environmental Sciences), were examined for antimicrobial
susceptibility and pulsed-field gel electrophoresis (PFGE)
pattern and compared with 4 isolates from 3 outbreaks in
Osaka Prefecture in 2003 and 2 isolates from sporadic cases
also in Osaka. The drug resistance pattern obtained by using
BD Sensi-Disc antimicrobial discs (Becton Dickinson Micro-
biology Systems, Cockeysville, Md., USA) following the
NCCLS guideline of the United States (6) revealed that all
the 49 isolates from the present outbreak were resistant to
ampicillin, chloramphenicol, streptomycin, sulfisoxazole, and
tetracycline (ACSSuT), and one isolate from a sporadic case
showed the same drug resistance pattern (Table 1). Eight
isolates from the institutions, 5 isolates from kindergartens,
4 isolates from other outbreaks and 2 isolates from sporadic
cases were submitted to the PFGE analysis of the total DNA
(7). All the isolates from the present outbreak and one isolate
from a sporadic case showed the same pattern, i.e., Ba type
in BlnI digestion and Xa pattern in XbaI digestion (both
restriction enzymes were products of Roche Diagnostics,
Mannheim, Germany) (Fig. 1). Other isolates showed dis-
similar patterns. Five isolates each from the institutions and
kindergartens and one isolate from a sporadic case were used
for bacteriophage typing (8). All 10 isolates from the present
outbreaks were typed as DT104, but the sporadic isolate was
typed as DT104B.
Most S. Typhimurium DT104 isolates implicated in food
poisoning in Europe and the United States were resistant to
ACSSuT, and the resistance genes were clustered within 13 kb
on the chromosome (9). The isolates from the present out-
break also showed the same drug resistance pattern, although
the isolates from other outbreaks in 2003 had a different drug
One isolate from a sporadic case in 2003 shared the same
drug resistance and PFGE patterns with the isolates from
the present outbreak. However, this isolate was DT104B,
rather than DT104 as in the present case. However, DT104B
is considered closely related to DT104; in fact, DT104B
isolates have been reported to have the same drug resist-
ance pattern (10) and PFGE pattern (11) as DT104 strains.
Jpn. J. Infect. Dis., 58, 2005
Our results suggest that close monitoring of DT104 S.
Typhimurium may be necessary.
The present investigation was supported by the grant-in-
aid of Ministry of Health, Labour and Welfare for Research
on Emerging and Re-emerging infections. The PFGE standard
strain Salmonella enterica serovar Braenderup H9812 was
obtained from USCDC PulseNet, and the phage typing set
from UK HPA (Health Protection Agency).
We thank Prof. H. Yoshikura, Emeritus member of National
Institute of Infectious Diseases, for advice on preparing the
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Fig. 1. PFGE patterns of S. Typhimurium isolates. Lanes 1, 9 and 17:
DNA size standard Salmonella enterica serovar Braenderup H9812;
lanes 2 and 10: an isolate from the institutions implicated in the present
outbreak; lanes 3 and 11: an isolate from the kindergartens implicated
in the present outbreak; 4 and 12, 5 and 13, and 6 and 14: isolates
from other outbreaks, B-D; 7 and 15, and 8 and 16: isolates from
Table 1. Characteristics of S. Typhimurium isolates in 2003 analyzed in the present report
Antimicrobial susceptibilityPFGE Bacteriophage typing
Case No. Outbreak monthImplicated food
No. of TypeType No. of
isolatesby by isolates Phage type
Food poisoning A September (Institutions)
8 ACSSuT8 Ba Xa5 DT104
41ACSSuT5 Ba Xa5 DT104
Food poisoning BSeptembernot identified 1sensitive1BbXb not done
Food poisoning C Augustnot identified 1STmSuT1 BcXcnot done
Food poisoning D Augustnot identified 2sensitive2 Bd Xdnot done
Sporadic case AJuly not identified 1ACSSuT1 BaXa1 DT104B
Sporadic case BOctobernot identified 1 KT1 BeXenot done
1): A, ampicillin; C, chloramphenicol; S, streptomycin; Tm, trimethoprim; Su, sulfisoxazole; K, kanamycin; T, tetracycline.