overview of listeria monocytogenes contamination in japan

10
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 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 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). www.elsevier.com/locate/ijfoodmicro International Journal of Food Microbiology 93 (2004) 131 – 140

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Page 1: Overview of Listeria monocytogenes contamination in Japan

www.elsevier.com/locate/ijfoodmicro

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

Page 2: Overview of Listeria monocytogenes contamination in Japan

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)

Page 3: Overview of Listeria monocytogenes contamination in Japan

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)

Page 4: Overview of Listeria monocytogenes contamination in Japan

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)

Page 5: Overview of Listeria monocytogenes contamination in Japan

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)

Page 6: Overview of Listeria monocytogenes contamination in Japan

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

Page 7: Overview of Listeria monocytogenes contamination in Japan

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-

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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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