overview of listeria monocytogenes contamination in japan
TRANSCRIPT
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International Journal of Food Microbiology 93 (2004) 131–140
Review
Overview of Listeria monocytogenes contamination in Japan
Akiko Okutani, Yumiko Okada, Shigeki Yamamoto, Shizunobu Igimi*
Division of Biomedical Food Research, National Institute of Health Sciences, 1-18-1, Kamiyoga, Setagaya, 158-8501, Tokyo, Japan
Received 27 February 2003; received in revised form 4 July 2003; accepted 11 November 2003
Abstract
Listeriosis is a relatively rare foodborne illness but can be life threatening with high fatality rates. In Japan, the
incidence of listeriosis has been very low for the past 40 years compared with that of Western Europe and North America.
We hypothesized that less Listeria monocytogenes contamination in Japanese foods would be related to the lower incidence
in Japan. For this purpose, we collected data of Japanese foods contaminated with L. monocytogenes, mainly from
Japanese-written reports, and reviewed them. From this review, we found that the proportion of L. monocytogenes, Listeria
spp. isolation from foods in Japan is similar to those reported from other countries and that other factors might be
responsible for the lower occurrence of listeriosis.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Listeria monocytogenes; Literature review; Japan; Food contamination; Listeriosis
1. Introduction
Listeria monocytogenes is a widely distributed
bacterium in nature and causes listeriosis in human,
such as meningitis and bacteremia, with high case
fatality. The infection is found mostly in neonates,
pregnant women and immunocompromised patients.
Since 1983, major foodborne listeriosis outbreaks
have been reported in Europe and North America
(Allerberger and Guggenbichler, 1989; Salamina et
al., 1996; Tham et al., 2000), mainly due to ready-
to-eat foods. To investigate the source or route of
infection, it is important to know which kinds of
foods are contaminated with L. monocytogenes and
0168-1605/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2003.11.014
* Corresponding author. Tel.: +81-3-3700-9164; fax: +81-3-
3700-9246.
E-mail address: [email protected] (S. Igimi).
its frequency and dose. Using scientific reports, the
FAO/WHO has been performing risk assessment of
L. monocytogenes in ready-to-eat foods.
The incidence of listeriosis in Japan has remained
very low and we have not experienced listeriosis
outbreaks. Terao (1990) reported the annual number
of listeriosis patients in Japan from 1958 to 1988. In
1958, 2 cases were reported and the number gradu-
ally increased to 62 cases in 1982. Since then the
number decreased to 19 cases in 1988. We have
estimated the recent incidence of listeriosis in Japan
by active surveillance (Okutani et al., 2004). Infor-
mation about L. monocytogenes infection was col-
lected by contacting clinical and laboratorial
specialists in each of the 2258 out of 9266 hospitals
in Japan. They were asked to indicate, retrospective-
ly, a rough estimate of the number of bacterial
meningitis patients and all the patients with listerio-
sis or all the L. monocytogenes isolates. From 1996
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140132
to 2002, 95 cases have been reported. The annual
number of cases is 83, calculated by the proportion
of the number of beds of replied hospitals. We
estimated the incidence of listeriosis per year in
Table 1
The proportion of L. monocytogenes, Listeria spp. isolation for meat
Number of samples
contaminated with
L. monocytogenes (%)
Number o
contamina
other Liste
Beef whole pieces 217/4231 (5.1) 708/3991
Beef sliced 101/378 (27) 12/100 (12
Beef minced 11/49 (22) 4/5 (80)
Minced beef–pork 16/51 (31) N.D.a
Beef liver 4/26 (15) N.D.
Beef (imported) 8/63 (13) 10/63 (16)
Pork whole pieces 355/4421 (8.0) 469/4365
Pork sliced 128/397 (32) 10/82 (12)
Pork minced 20/104 (19) 20/67 (30)
Pork entrails 3/43 (7.0) 11/37 (30)
Pork (imported) 2/59 (3.4) 10/54 (19)
Chicken whole parts 49/331 (15) 76/291 (26
Chicken sliced 140/350 (40) 1/4 (25)
Chicken minced 22/53 (42) 5/6 (83)
Chicken giblets 2/3 (67) N.D.
Horseflesh sliced 15/503 (3.0) N.D.
a No data.
Japan as 0.65 per one million inhabitants (the whole
population of Japan in year 2000 was 126,925,843).
Compared with this, the U.S Centers for Disease
Control and Prevention (CDC)’s Emerging Infections
f samples
ted with
ria spp. (%)
References
(18) (Katayama et al., 1991a; Ono et al.,
1993; Ryu et al., 1992; Takagi et al.,
1989a,b; The National Meat Inspection
Committee, 1992)
) (Handa et al., 1989; Iida et al., 1998;
Katayama et al., 1991a; Masuyama,
1991; Ryu et al., 1992; Takagi et al.,
1989a,b)
(Inoue et al., 2000a,b; Ryu et al., 1992;
Takagi et al., 1989a,b)
(Inoue et al., 2000a,b; Kumon et al., 1999)
(Kumon et al., 1999, 2000)
(Handa et al., 1989; Hyakutake, 1994;
Kyoto-shi Eisei Kougai Kenkyujo
Nenpo, 1991)
(11) (Katayama et al., 1991a; Ono et al., 1993;
Ryu et al., 1992; The National
Meat Inspection Committee, 1992;
Yamanaka et al., 1993)
(Handa et al., 1989; Iida et al., 1998;
Katayama et al., 1991a; Masuyama,
1991; Ryu et al., 1992; Takagi et al.,
1989a,b)
(Handa et al., 1989; Inoue et al., 2000a,
b; Ryu et al., 1992; Takagi et al., 1989a,b)
(Handa et al., 1989; Machida, 1993;
Takagi et al., 1989a,b)
(Handa et al., 1989; Hyakutake, 1994;
Machida, 1993)
) (Handa et al., 1989; Inoue et al., 2000a,b;
Katayama et al., 1991a; Kyoto-shi Eisei
Kougai Kenkyujo Nenpo, 1991; Ono et al.,
1993; Ryu et al., 1992; Takagi et al.,
1989a,b; Ueno et al., 1995/1996; Yamanaka
et al., 1993)
(Iida et al., 1998; Ryu et al., 1992; Takagi
et al., 1989a,b)
(Inoue et al., 2000a,b; Ryu et al., 1992;
Takagi et al., 1989a,b)
(Takagi et al., 1989a,b
(Handa et al., 1989; Iida et al., 1998; Takagi
et al., 1989a,b)
Table 2
The proportion of L. monocytogenes, Listeria spp. isolation for
natural cheese
Number of
samples
contaminated
with L.
monocytogenes
(%)
Number of
samples
contaminated
with other
Listeria spp.
(%)
References
Raw milk 7/139 (5.0) 4/52 (7.7) (Takeshi et al.,
1992, 1994)
Cheese
ingredient
0/19 (0) 0/19 (0) (Nakama et al.,
1993b)
Retail cheese 0/5 (0) N.D.a (Handa et al.,
1989)
Natural cheese
(domestic)
0/1075 (0) 0/64 (0) (Nakama et al.,
1993a; Takeshi
et al., 1992, 1994)
Natural cheese
(imported)
33/1387 (2.4) 4/245 (1.6) (Kitazume et al.,
1991; Nakama
et al., 1993a; Ryu
et al., 1992)
a No data.
Table 3
The proportion of L. monocytogenes and Listeria spp. isolation for seafoo
Number of samples
contaminated with
L. monocytogenes (%)
Number of sa
contaminated
other Listeria
Fresh seafood 41/2659 (1.5) 141/1399 (10)
Processed seafood 21/526 (4.0) 21/279 (7.5)
Frozen seafood 0/6 (0) 1/6 (17)
Ark shell 2/20 (10) 2/20 (10)
Clam 0/9 (0) 7/9 (78)
Kabayaki 0/22 (0) 4/22 (18)
Spithcock 0/18 (0) N.D.a
Shirayaki 1/26 (3.8) 4/26 (15)
Raw oyster 0/46 (0) 0/46 (0)
Oyster 0/25 (0) 0/25 (0)
Smoked salmon 5/92 (5.4) N.D.
Cockle 0/3 (0) 2/3 (67)
Young yellowtail 0/6 (0) 0/6 (0)
Flat fish 0/2 (0) 0/2 (0)
Scallop 1/21 (4.8) 2/21 (9.5)
Red sea bream 0/1 (0) 0/1 (0)
Raw minced tuna 3/37 (8.1) 16/37 (43)
Raw prawn 1/38 (2.6) 6/38 (16)
Other raw seafoods 3/18 (17) 0/18 (0)
a No data.
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140 133
Program, Foodborne Diseases Active Surveillance
Network (FoodNet), indicated five reported cases
of listeriosis per million annually in United States
for the years from 1996 to 1998 (CDC, 1998). Mead
et al. (1999) estimated 2493 cases of listeriosis,
including 499 deaths using 1996–1997 surveillance
data and extrapolating to the 1997 total U.S. popu-
lation. Goulet et al. (2001) estimated the annual
number of cases due to L. monocytogenes to be
4.1 cases per million in 1997 in France.
No definitive evidence exists to explain these
differences, but several factors have been hypothe-
sized. Generally, if there are no or few routes of
infection, infectious disease cannot break out. In the
case of listeriosis, contaminated foods are the main
routes of infection; therefore, it might be possible
that foods in Japan are less contaminated than that
of countries which have had foodborne outbreak of
listeriosis. No verification has been performed yet
from this point of view, so we ascertained the
d
mples
with
spp. (%)
References
(Iida et al., 1998; Inoue et al., 2000a,b;
Kawasaki et al., 1992; Masuda et al.,
1992; Ogawa et al., 1992; Ryu et al., 1992)
(Iida et al., 1998; Kawasaki et al., 1992;
Ogawa et al., 1992; Ryu et al., 1992)
(Ogawa et al., 1992)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Masuda et al., 1991)
(Handa et al., 1989)
(Masuda et al., 1991)
(Ogawa et al., 1992)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Inoue et al., 2000a,b)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Ryu et al., 1992)
(Ryu et al., 1992)
(Ryu et al., 1992)
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140134
situation of L. monocytogenes contamination in
Japanese foods by literature review.
Many methodical reports of L. monocytogenes
contamination in Japanese foods have been pub-
lished since the Ministry of Health, Labor and
Welfare formed the guidelines for isolation of L.
monocytogenes from soft and soft type natural
cheese in 1988 (The Ministry of Health, Labour
and Welfare, 1988) because some European natural
cheese were found to be contaminated with L.
monocytogenes. We searched for reports which sur-
veyed the situation of Japanese retail food contam-
ination with L. monocytogenes by the keywords
Listeria, food, survey and Japan from a database of
Japan Science and Technology Corporation Online
Information System (JOIS). Many scientific and
reproducible reports were found but many of them
were written in Japanese and published in Japanese
journals, which made it difficult for non-Japanese
researchers to cite them. From these reports, we
made lists of the proportion of Japanese retail foods
contaminated with L. monocytogenes sorted by food
categories and analyzed the Japanese situation.
Table 4
The proportion of L. monocytogenes, Listeria spp. isolation for other read
Number of samples
contaminated with
L. monocytogenes (%)
Number of sampl
contaminated wit
other Listeria spp
Processed meat 0/64 (0) 0/64 (0)
Ham salad 1/8 (13) 0/8 (0)
Meat products 10/148 (6.8) 15/148 (10)
Roast beef 0/7 (0) 0/7 (0)
Ham 0/5 (0) 0/5 (0)
Ham 0/10 (0) 0/10 (0)
Raw pork ham 0/3 (0) 0/3 (0)
Milk and dairy foods 0/53 (0) 0/53 (0)
Cakes 0/154 (0) 0/154 (0)
Cakes 1/76 (1.3) 0/76 (0)
Noodle 0/47 (0) 1/47 (2.1)
Daily dishes 6/613 (1.0) 15/613 (2.4)
Lunch box 1/141 (0.7) 3/141 (2.1)
Potato salad 0/3 (0) 0/95 (0)
Bread 0/95 (0) 0/30 (0)
Liquid contents of eggs 0/30 (0) 3/30 (10)
Omelets 0/37 (0) 0/37 (0)
Bean curd (tofu) 0/20 (0) N.D.a
Others 0/59 (0) 0/59 (0)
Processed vegetables 1/386 (0.3) 0/101 (0)
a No data.
2. Food monitoring based on nationwide review
The reports describing surveys of L. monocytogenes
contaminations of retail food in Japan from 1988 to
present were collected. We selected 32 reports, which
described the use of Listeria enrichment broth (EB,
Merck, Germany) or UVM medium (Difco Laborato-
ries, USA) for enrichment and PALCAM agar medium
(Merck) or Oxford agar medium (Oxoid, UK) for
identification according to the International Dairy Fed-
eration (IDF) standard methods. They were mainly
from the annual reports of authorized institutions;
public health institutes in local, self-governing bodies
of Japan, and from Japanese journals written in Japa-
nese. Each retail food was classified by category to list
the prevalence of L. monocytogenes or Listeria spp.
3. Data analysis from the category lists
We classified foods into seven categories; meats,
natural cheese, seafood, other ready-to-eat foods, ani-
mals, humans, and environment.
y-to-eat foods
es
h
. (%)
References
(Ogawa et al., 1992)
(Takagi et al., 1989a,b)
(Mori et al., 1990)
(Ryu et al., 1992)
(Machida, 1993)
(Takagi et al., 1989a,b)
(Ryu et al., 1992)
(Ogawa et al., 1992)
(Ogawa et al., 1992)
(Masuda et al., 1991)
(Ogawa et al., 1992)
(Ogawa et al., 1992)
(Ogawa et al., 1992)
(Ryu et al., 1992)
(Ogawa et al., 1992)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Kyoto-shi Eisei Kougai Kenkyujo Nenpo, 1991)
(Handa et al., 1989)
(Ogawa et al., 1992)
(Inoue et al., 2000a,b; Kyoto-shi Eisei Kougai Kenkyujo
Nenpo, 1991; Ogawa et al., 1992; Ryu et al., 1992)
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140 135
The meat category included beef, pork, chicken
and horseflesh. We categorized each meat as whole
pieces, sliced, minced, parts of intestine, according
to processing methods, and imported, if possible.
We found that sliced and minced meat and parts of
intestine, which had been processed, showed higher
L. monocytogenes contamination than whole pieces
of meat (Table 1). Chicken showed higher levels
than other meats (Table 1).
In the cheese category (Table 2), Takeshi et al.
(1992, 1994) reported L. monocytogenes contami-
nation of raw milk. In Japan, the producer must
use pasteurized milk (62–65 jC, 30 min or
equivalent) for making natural cheese (The Minis-
try of Health, Labour and Welfare, 1993). There-
fore, even if milk was contaminated with L.
monocytogenes before pasteurization, it is reason-
able to assume that domestically produced cheeses
were Listeria-free (Table 2). Even though the
possibility of cross-contamination after pasteuriza-
tion could not be excluded, we could not find the
Table 5
The proportion of L. monocytogenes, Listeria spp. isolation for animals
Number of samples
contaminated with
L. monocytogenes (%)
Number of sam
contaminated w
other Listeria sp
Cattle feces 0/244 (0) 0/106 (0)
Cattle carcass surface 202/4106 (4.9) N.D.a
Cattle swab of surface 1/31 (3.2) 3/31 (9.7)
Cattle intestinal contents 394/19134 (2.1) 439/9337 (4.7)
Swine feces 0/393 (0) 4/393 (1.0)
Swine carcass surface 321/4330 (7.4) N.D.
Swine swab of surface 8/32 (25) 11/32 (34)
Swine intestinal contents 95/11829 (0.8) 380/5687 (6.7)
Swabs of chicken body 0/15 (0) N.D.
Chicken feces 0/150 (0) N.D.
Horse intestinal contents 0/376 (0) 36/376 (9.6)
Sheep intestinal contents 2/83 (2.4) 6/83 (7.2)
Goat intestinal contents 0/42 (0) 0/42 (0)
Dog feces 6/611 (1.0) 0/71 (0)
Cat feces 1/44 (2.3) 0/43 (0)
Rat 0/9 (0) 1/9 (11.1)
Rat intestinal contents 13/199 (6.5) N.D.
Wild boar 0/17 (0) 1/17 (5.9)
Racoon dogs 4/108 (3.7) 40/108 (37)
Fish intestine contents 3/16 (19) 1/16 (6.3)
a No data.
case of cross-contamination in this survey. Sea-
food, which Japanese commonly eat, often raw,
was not highly contaminated with L. monocyto-
genes. The proportion of L. monocytogenes con-
tamination of fresh and processed seafood was less
than 10%. Individual seafood products were also
contaminated less than 10% as shown in Table 3.
The other ready-to-eat foods category included a
wide variety of foods which are edible without
heating. While dairy foods, egg products and other
foods had low contamination levels, meat products
were rather more contaminated; 6.8% and 13%
(Table 4).
Apart from swine swab of surface, contamina-
tion levels of feces, carcasses and intestinal con-
tents were low (Table 5). Wild animals, except
livestock, in the animal category were contaminated
with L. monocytogenes at low levels (Table 5).
Intestine of fish living in the water around slaugh-
terhouses had relatively high L. monocytogenes
contamination; 19% (Table 5). We found that feces
ples
ith
p. (%)
References
(Handa et al., 1989; Inoue et al., 2000a,b)
(Iida et al., 1998)
(Masuyama, 1991)
(Iida et al., 1998; Katayama et al., 1990; Masuyama,
1991; The National Meat Inspection Committee, 1991)
(Handa et al., 1989; Inoue et al., 2000a,b)
(Iida et al., 1998)
(Masuyama, 1991)
(Iida et al., 1998; Katayama et al., 1990; Masuyama,
1991; The National Meat Inspection Committee, 1991)
(Handa et al., 1989)
(Handa et al., 1989)
(The National Meat Inspection Committee, 1991)
(The National Meat Inspection Committee, 1991)
(The National Meat Inspection Committee, 1991)
(Iida et al., 1998; Inoue et al., 2000a,b)
(Handa et al., 1989; Inoue et al., 2000a,b)
(Katayama et al., 1991b)
(Iida et al., 1998)
(Katayama et al., 1991b)
(Katayama et al., 1991b)
(Momose, 1991)
Table 7
The proportion of L. monocytogenes, Listeria spp. isolation for
environmental samples
Number of
samples
contaminated
with L.
monocytogenes
(%)
Number of
samples
contaminated
with other
Listeria spp.
(%)
References
Moorings
for swine
0/2 (0) 1/2 (50) (Momose,
1991)
Disassembling
place for
swine
3/6 (50) 5/6 (83) (Momose,
1991)
Disassembling
place for
cattle
1/5 (20) 3/5 (60) (Momose,
1991)
Materials from
clean rooms
5/74 (6.8) 4/74 (5.4) (Machida,
1993;
Nakama
et al., 1993b)
Utensils 1/399 (0.3) 4/395 (1.0) (Handa et al.,
1989; Ogawa
et al., 1992)
Truck for
transportation
1/33 (3.0) 0/33 (0) (Masuyama,
1991)
Food of chicken 0/27 (0) N.D.a (Handa et al.,
1989)
Sludge 9/103 (8.7) N.D. (Katayama
et al., 1990;
Takeshi
et al., 1994)
Sewage 12/283 (4.2) 43/274 (16) (Handa et al.,
1989;
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140136
of workers at slaughterhouses showed the same
contamination levels as that of healthy volunteers,
around 1% and swabs of hands and fingers of
workers were not contaminated with L. monocyto-
genes (Table 6). From these data, we could not
find clear evidence that the workers at slaughter-
houses owe L. monocytogenes contamination dur-
ing the process. It is important to check the
contamination level of the environment at slaugh-
terhouse because high contamination of processed
foods might be caused by contaminated facilities
(Miettinen et al., 2001; Norrung, 2000; Notermans
and Hoornstra, 2000). In Table 7, disassembling
places at slaughterhouses were contaminated at
20% and 50% (Momose, 1991). Contaminated
utensils and environment could be one of the
routes of contamination.
The amount of L. monocytogenes in contaminat-
ed samples was seldom mentioned in the literature.
Two reports noted these amounts, and the majority
of the foods had less than 100/g (MPN) of L.
monocytogenes (Inoue et al., 2000a,b; Nakama et
al., 1993b), except minced chicken, which showed
contamination levels higher than 100/g (MPN)
(Inoue et al., 2000a,b).
Eleven reports listed the serotypes of L. mono-
cytogenes isolates from domestic foods and the
environment (Table 8). From the meat and ready-
to-eat categories, serotype 1/2a, 1/2b and 1/2c
Table 6
The proportion of L. monocytogenes, Listeria spp. isolation for
humans
Number of
samples
contaminated
with L.
monocytogenes
(%)
Number of
samples
contaminated
with other
Listeria spp.
(%)
References
Healthy
human feces
38/2970 (1.3) N.D.a (Iida et al.,
1998)
Feces of workers at
slaughterhouses
4/265 (1.5) N.D. (Takagi
et al.,
1989a,b)
Swab of hands and
fingers of
workers
0/257 (0) 3/257 (1.2) (Ogawa
et al.,
1992)
a No Data.
Masuyama,
1991;
Momose,
1991; Ogawa
et al., 1992;
Takeshi et al.,
1992)
Silage 0/7 (0) N.D. (Takeshi et al.,
1994)
a No data.
demonstrated similar numbers of isolates and were
the most commonly reported serotypes. The number
of serotype 4b isolates from these categories was
about half the number of the serotypes listed above.
Other serotypes were rarely reported. From the
categories of environment, feces and animals, sero-
type 1/2c was the most frequently reported. This
serotype was isolated mainly from the carcass
Table 8
The list of serotypes of L. monocytogenes from domestic foods and environment
Serovar References
1/2a 1/2b 1/2c 3a 3b 4a 4b 4c 4e 6a (4f) Other
Meat
Beef whole pieces 2a 2 2 2 (Ono et al., 1993)
Beef sliced 12 12 33 1 18 1 4 (Handa et al., 1989; Iida et al., 1998)
Beef minced 3 2 1 1 (Inoue et al., 2000a,b)
Beef entrails 2 2 1 1 (Kumon et al., 1999, 2000)
Pork whole pieces 1 7 4 1 2 (Ono et al., 1993; Yamanaka et al., 1993)
Pork sliced 11 16 42 6 1 (Iida et al., 1998)
Pork minced 4 2 4 3 2 8 1 (Handa et al., 1989; Inoue et al., 2000a,b)
Minced beef–pork 7 8 9 6 1 (Inoue et al., 2000a,b; Kumon et al., 1999)
Pork entrails 3 3 (Handa et al., 1989)
Chicken whole parts 6 3 2 2 (Ono et al., 1993; Yamanaka et al., 1993)
Chicken sliced 49 27 31 15 1 (Iida et al., 1998)
Chicken minced 4 11 4 (Inoue et al., 2000a,b)
Horseflesh sliced 5 5 4 1 (Iida et al., 1998)
Ready-to-eat
Fresh seafood 14 13 1 2 13 3 (Iida et al., 1998; Inoue et al., 2000a,b;
Kawasaki et al., 1992; Masuda et al., 1992)
Processed seafood 7 5 1 (Iida et al., 1998)
Smoked salmon 2 2 1 (Inoue et al., 2000a,b)
Shred-type cheese 9 (Nakama et al., 1993b)
Sub total 127 124 134 1 2 6 69 1 0 12 19
Environment
Sewage 1 (Handa et al., 1989)
Materials from clean rooms 5 (Nakama et al., 1993b)
Feces
Healthy human feces 17 9 10 2 (Iida et al., 1998)
Dog feces 1 1 2 2 (Iida et al., 1998; Inoue et al., 2000a,b)
Cat feces 1 (Inoue et al., 2000a,b)
Swine feces 3 (Handa et al., 1989)
Animals
Cattle carcass surface 3 11 179 3 6 (Iida et al., 1998)
Swine carcass surface 18 26 265 9 3 (Iida et al., 1998)
Cattle intestinal contents 4 12 150 3 1 20 (Iida et al., 1998)
Swine intestinal contents 11 15 5 1 14 (Iida et al., 1998)
Rat intestinal contents 2 4 1 2 4 (Iida et al., 1998)
Sub total 57 82 601 0 0 0 30 0 1 4 51
Total 184 206 735 1 2 6 99 1 1 16 70
a Number of isolates.
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140 137
surface of cattle and swine, and also from cattle
intestinal contents.
4. Conclusion
There are many reports about the levels of con-
tamination with L. monocytogenes in ready-to-eat
foods in western countries. According to the survey
of L. monocytogenes in ready-to-eat foods in US, the
overall prevalence was reported as 1.82%, ranging
from 0.17% to 4.7% (Gombas et al., 2003). In
France, total proportion of ready-to-eat foods con-
taminated with L. monocytogenes from 1995 to 1996
was 6.7% (Goulet et al., 2001). The incidence of L.
monocytogenes in imported seafood products in
Canada was 0.88% (1996–1997) and 0.3% (1997–
1998) (Farber, 2000).
We found that many research groups in Japan
have surveyed food contamination with L. monocy-
A. Okutani et al. / International Journal of Food Microbiology 93 (2004) 131–140138
togenes and reported the potential of these foods to
cause listeriosis. However, administrative regulation
has not been based on the recognition of listeriosis
as a foodborne disease and there has been little
consensus among Japanese that listeriosis is a food-
borne disease. This may be a result of the low
incidence of listeriosis in Japan, and therefore, we
considered it was necessary to search the frequency
of L. monocytogenes contamination in Japan in
comparison with other countries. From this review,
we found that a wide variety of foods were contam-
inated with L. monocytogenes in Japan.
Each type of contaminated food had different
potentials to cause listeriosis. In the meat categories,
the contamination was high (Table 1), but the risk to
infect with L. monocytogenes would be low because
we usually eat them after cooking. However, ham
and meat products (Table 4), which are edible
without heating, have to be carefully treated during
processing and transportation to prevent contamina-
tion. It is believed that the frequency and concentra-
tion of L. monocytogenes contamination become
higher through the food processing procedure (Noter-
mans and Hoornstra, 2000); therefore, proper super-
vision of processing procedures to maintain hygiene
and to prevent cross-contamination is important.
Though data in Table 7 were limited, we seized an
opportunity to evaluate which steps of the proce-
dures should be controlled to prevent contamination
and recontamination of foods with L. monocytogenes
while processing. As the FAO/WHO working group
concluded that ‘the total elimination of L. monocy-
togenes from all food is impractical and may be
impossible’ (FAO/WHO working Group, 1988), a
strong control system to minimize L. monocytogenes
contamination from production to consumption must
be maintained. Both frequency and levels of con-
tamination data are needed to evaluate the relation-
ship between contamination and listeriosis, but the
data from this study of L. monocytogenes-positive
foods did not reveal a correlation because most
papers did not report levels of contamination data.
In Table 8, serotype 1/2c was the most widely
distributed serotype found in foods, environment and
animals. However, although 1/2c comprised the ma-
jority in foods and the environment, this serotype was
seldom isolated from clinical samples in Japan. These
circumstances are not limited to Japan. Kathariou
(2002) suggested that certain resident clones in the
processing plant (e.g., those of serotype 1/2c) are not
commonly implicated in human illness, while others
(1/2a, 1/2b and 4b) clearly have the potential to cause
human listeriosis, depending on their serotype and
contamination level in the product.
Serotype 4b, which has been most frequently
isolated from listeriosis patients (Farber and Peterkin,
1991; Terao, 1991), was not the predominant sero-
type of food and environmental isolates in Japan
(Table 8). Serotype 4b was not the leading serotype
among food isolates in the western countries either,
as Greenwood et al. (1991) and Hayes et al. (1991)
reported. Kathariou (2002) suggested that this dis-
crepancy between food incidence and prevalence in
illness may be because serotype 4b is more virulent
to humans than other serotypes, but the details
remain unclear. Serotype 1/2a and 1/2b, noted to
be linked to listeriosis as well, were equally detected
in meat and animal samples (Table 8). These sero-
types are also reported to cause human illness as
serotype 1/2a was the strain implicated in the US
outbreak involving contaminated turkey deli meat
(CDC, 2000), and 1/2b was found in 10% of all
listeriosis cases by McLauchlin (1990).
We could not find a direct relationship between the
proportion of food contaminated with L. monocyto-
genes, which was almost the same as that of other
countries, and the low incidence of listeriosis in Japan.
We have to find the other factors to analyze this
contradiction. However, we conclude that this report
provides referable data of the Japanese situation of
food contamination with L. monocytogenes for
researchers from other countries to cite.
Acknowledgements
This work was supported by Health and Labour
Sciences Grants, Research on Food and Chemical
Safety.
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