Sushi
and sashimi exhibit distinct features that are
associated with introduction of microbiological
hazards. In the past three years, 3% of reported
food poisoning outbreaks have been associated
with sushi and sashimi and have resulted in 142
affected persons. The Food Surveillance Programme
took a total of 1020 sushi and 906 sashimi samples
from 1997 through 1999 for microbiological assessment
and evaluated against the microbiological guidelines
of FEHD. Among these samples, 13.8% of sushi and
11.1% of sashimi were unsatisfactory in terms
of their hygienic quality and 0.26% of all samples
yielded specific pathogens including one Vibrio
parahaemolyticus, two Staphlococcus aureaus,
one Salmonella species, and one Listeria
Monocytogenes. Both the product quality as
well as safety could be improved by incorporating
safety measures throughout the manufacturing process,
such as by adopting the Good Manufacturing Practice
and Hazard Analysis Critical Control Point system.
Sushi and
sashimi have been among the popular food items in Hong
Kong. They are not only found in the conventional Japanese-style
restaurants, but also a variety of food premises that
serve Chinese and Western dishes. Sushi and sashimi are
also sold in self-service Sushi Restaurants. Different
types of sushi and sashimi are produced and displayed,
typically on conveying belts, and the customers simply
need to pick up the ones they want. Pre-packed sushi and
sashimi are available in the supermarkets, or shops on
main streets or in shopping centres. Importers, food manufacturers,
restaurant owners and even supermarket entrepreneurs have
been attracted to participate in these varieties of business.
The objective of this study
is to evaluate the microbiological hazards associated
with sushi and sashimi in Hong Kong. In this paper, we
first define the issue, followed by a review of the production
process of sushi and sashimi to identify features that
are associated with introduction of microbiological hazards.
The microbiological surveillance results of sushi and
sashimi from 1997 to 1999 in Hong Kong are then presented
and analysed. Recommendations on reduction of microbiological
hazards in sushi and sashimi are put forward to the trade
and the public.
Sushi and
Sashimi are classified as restricted food in the Food
Business Regulation of the Public Health and Municipal
Services Ordinance (Chapter 132). It has been defined
that ¡§Sashimi¡¨ is
food consisting of fillets of marine fish, molluscs, crustaceans,
fish roe or other seafood to be eaten in its raw state.
Under the same Regulations, ¡§sushi¡¨ refers
to food consisting of cooked and pressed rice flavoured
with vinegar and garnished with other food ingredients
including raw or cooked or vinegared seafood, marine fish
or shellfish roe, vegetable, cooked meat or egg on top
or in the middle which may or may not be wrapped with
seaweed and usually served in pieces.
Microbiological
hazards
Micro-organisms
include bacteria, viruses, yeasts and moulds. Not all
of them are harmful. Those capable of causing foodborne
illness are known as foodborne pathogens. Some others
may cause food spoilage with colour and flavour degradation.
As regards foodborne pathogens, some of them may be carried
in raw food and persist throughout the food preparation
process. For instance, Vibrio parahaemolyticus is
commonly found in seafood, whereas Staphylococcus aureus
and Salmonella species may be introduced into
food by cross-contamination or improper handling during
food processing.
Microbiological
assessment of sushi and sashimi provides information regarding
the hygienic quality and product safety. The most commonly
adopted initial assessment is through a determination
of the number of indicator organisms in food. The number
of aerobic bacteria colonies grown in the laboratory conditions,
technically termed as Aerobic Plate Count (APC), has been
used to assess product quality. In terms of food safety,
the commonest indicator organism employed is Escherichia
coli (E. coli) which reflects the extent of
faecal contamination and the possible presence of enteric
pathogens in foods. There are limitations associated with
each of these tests but the results will in general give
some indications on the standard of hygienic practice
in food preparation and storage. The International Commission
on Microbiological Specifications for Foods (ICMSF) has
indicated in 1978 that the presence of E. coli
in a food does not connote directly the presence of a
pathogen, but only implies a certain risk that it may
be present. In other words, the measurements may not be
associated with human illnesses directly (1).
Food
poisoning outbreaks due to consumption of sushi and sashimi
From 1997 to 1999, food
poisoning outbreaks due to consumption of sushi and sashimi
accounted for 3.0% (45 out of 1481) of all food poisoning
outbreaks reported to the Department of Health. A total
of 142 persons (1.8% of 7728) were affected in these outbreaks.
The three commonest causative bacteria identified were
Vibrio parahaemolyticus (28 outbreaks affecting
100 people), Staphylococcus aureus (7 outbreaks
affecting 17 people), and Salmonella species (5
outbreaks affecting 15 people). Of these outbreaks, 15
of them (33.3%) were due to consumption of sushi and the
rest (66.7%) were caused by sashimi. (Source of Data:
Department of Health)
To evaluate
microbiological hazards associated with sushi and sashimi,
it is necessary to first review how these food items are
being produced. Generally speaking, the production process
of sushi and sashimi can be divided into four principal
stages: purchasing, storage, preparation, and delivery
& display (Figure 1). The
following paragraphs highlight the special features of
these steps and identify features that are associated
with microbiological hazards.
Purchasing
Seafood
is the key ingredient of sashimi, and to a large extent,
of sushi as well. The most commonly used seafood for sushi
and sashimi are salmon, tuna, octopus, yellow tail, and
hokkigai. They are mostly imported from abroad by air
and by sea. For instance, Norway has contributed to around
75% of total imported salmon in 1998 (2).
For sushi,
ingredients other than marine products may be used. Examples
include fried soybean cakes, sweet omelette, and cucumber.
It is crucial
for the manufacturers to obtain good quality ingredients,
as these food items will be consumed raw after preparation.
They should be purchased from reliable and reputable sources,
and preferably with health certificate issued by competent
authority of the country of origin.
Storage
As the frozen
or chilled seafood arrives at the manufacturing area in
central factories and/or outlets, they are checked and
then stored in freezer or refrigerator to maintain required
temperature. For frozen products, they should be kept
at or below -18¢XC until the day prior to preparation. Prolonged storage
is possible at this temperature when micro-organisms remain
dormant and unable to multiply. Chilled storage refers
to keeping the food at a temperature between 0-4¢XC. At this temperature range,
the growth of most bacteria can be prevented but some
pathogens, notably Listeria monocytogenes and a
wide variety of food spoilage organisms, may grow slowly.(3)
Food spoilage is therefore possible as enzyme activity
may still occur at down to -10¢XC(4).
Preparation
Frozen seafood
is usually defrosted in the refrigerator (<
4¢XC) one day before preparation. On the day of preparation, the seafood
is washed and then cut into the desired shape such as
fillets, slices or cubes. They can be immediately served
as sashimi, like salmon sashimi and tuna sashimi.
Preparation
of rice is a major step in sushi processing. Rice is cooked,
cooled and then treated with seasonings such as vinegar
and sugar. If it is not used immediately, they may be
put in the refrigerator temporarily, otherwise the shari
(vinegared rice) is pressed or moulded into the desired
shape, usually as a rice cube weighing 25-30g. This may
be done by an automatic moulder, or by hand, depending
on the scale of the food premises. Seafood slice is then
added on the rice cube so as to be served as seafood sushi.
This style of sushi is called as ¡§Nigiri-Sushi¡¨.
There are
other types of sushi (¡§Maki-Sushi¡¨
& ¡§Oshi-Sushi¡¨) with additional ingredients like
seaweed and cucumber that may require more handling. They
may be pressed hard, rolled tight and cut. Again, they
may be served immediately or chilled (< 4¢XC) during transportation
or display.
Delivery
and/or display
Well-prepared
sushi and sashimi are placed on plates and properly covered
before serving or packed in plastic box for display. Some
operators may prefer to pack sushi by plastic paper individually.
To minimize any potential bacterial multiplication, the
finished sushi and sashimi should be stored at or below
4¢XC
during display or transportation.
Features
associated with introduction of microbiological hazards
Sushi and sashimi and their
preparation processes carry specific features that may
be associated with introduction of microbiological hazards.
Firstly, most ingredients used for sushi and sashimi are
eaten raw and cold. Secondly, cooked ingredients are not
reheated prior to serving. Thirdly, the storage temperature,
if not properly maintained, could contribute to growth
and persistence of micro-organisms. And fourthly, the
preparation involves many handling steps by bare hands.
The practice of food handlers therefore plays a crucial
role in determining the hygienic status of the final products.
In Hong
Kong, food premises holding a general restaurant or food
factory license have to obtain specific endorsement for
manufacturing and sale of sushi and sashimi. Others who
want to sell but not manufacture sushi and sashimi also
need to obtain a special permit. As of January 2000, some
770 premises have been issued licenses with such endorsement
or permits. Under the Food Surveillance Programme, sushi
and sashimi samples are collected at the point of sale
from these outlets for microbiological assessment. The
following presents an analysis on the surveillance findings
from 1997 through 1999.
Methods
& laboratory determination
Under the
current arrangement, Food Inspectors are responsible for
taking food samples and send them to the Public Health
Laboratories, Pathology Service of the Department of Health
for microbiological analysis. Between January 1997 and
December 1999, a total of 1,926 samples (Table
1) of sushi and sashimi from different outlets were
collected for microbiological examination.
The laboratory
determination consists of two parts. The first part is
an assessment on the level of indicator organisms (APC
& E. coli (total)) and the other on specific
pathogens including Salmonella species, Shigella
species, Staphylococcus aureus, and Vibrio parahaemolyticus.
Results
The Microbiological
Guidelines for Ready-to-eat Food of the Food and Environmental
Hygiene Department is used as the reference for the food
surveillance. The microbiological guidelines for sushi
and sashimi are shown in Appendix
1.
Hygienic
Quality
APC or E.
coli (total) can reflect the general hygienic status
of sushi and sashimi. From 1997 through 1999, 13.8% (141
out of 1020) of sushi and 11.1% (101 out of 906) of sashimi
samples were found unsatisfactory (Tables 2
and 3).
Trend analysis
showed that there had been improvement in the hygienic
quality of sashimi, with a progressive decrease in the
unsatisfactory proportion from 17.5% in 1997 to 10.1%
and 4.3% in 1998 and 1999. For sushi, improvement had
occurred mainly in 1999, with the unsatisfactory rates
at 15.4%,18.4%, and 8.5% in 1997 to 1999. (Figures 2
and 3)
Specific
Pathogens in Sushi
Among the
1020 sushi samples examined, two were found to contain
pathogen - Staphylococcus aureus. For these two,
one was detected in 1997 in a California Maki and the
other in tuna fish sushi sampled in 1999.
Specific
Pathogens in Sashimi
Among the
906 samples of sashimi examined, three samples were found
to contain food poisoning pathogens. In 1998, two sashimi
samples yielded Vibrio parahaemolyticus and Listeria
monocytogenes each. The former was in a shrimp sashimi
whereas the latter in a flying fish roe sashimi. In 1999,
one salmon sashimi grew Salmonella species.
Interpretation
of findings
High levels
of APC and E. coli (total) are indicative of unsatisfactory
hygienic practice during processing of food from source
to table. High counts of APC in foods often indicate contaminated
raw materials or unsatisfactory processing and indicate
unsuitable time/temperature conditions during storage
(1). Although these organisms may not
directly cause human illness, the levels of unsatisfactory
samples suggested room for improvement in the production
process.
Specific pathogens had been
isolated in only a small proportion (0.26%) of the sushi
and sashimi samples taken in the past three years. Four
pathogenic organisms, namely Vibrio parahaemolyticus,
Staphylococcus aureus, Salmonella species and
Listeria monocytogenes, were identified. Vibrio
parahaemolyticus is commonly found in seafood. It
might persist and multiply as a result of improper hygienic
practice. Staphylococcus aureus and Salmonella
species might be introduced by the food handler, whereas
Salmonella species and Listeria monocytogenes
by cross-contamination of other foods. All of these pathogens
can cause gastrointestinal illness with symptoms of vomiting,
diarrhoea and abdominal pain occuring within the first
few days of ingestion. Listeria monocytogenes is
characterized by a longer incubation period, typically
3 weeks, and will cause severe illness in people with
impaired immunity such as the elderly, neonates, and pregnant
mothers.(5,6) These pathogens are described in more details in Appendix
2.
With effect
from 1 March 1997, all food premises engaged in the preparation
and/or sale of sushi and sashimi have been subject to
licensing control. The product safety is monitored regularly
by the Food Surveillance Programme. The legal provision
to control these food premises is detailed in Appendix 3.
Good Manufacturing
Practice (GMP) and Hazard Analysis and Critical Control
Point (HACCP) are both ways to incorporate food safety
control measures in the manufacturing process and may
contribute to strengthen food safety control.(7)
The following are recommendations for the trade derived
basing on the principles of GMP and HACCP.
The
trade to observe key steps in production
The trade
is recommended to pay special attention to the following
key steps:
Buy the seafood and other
raw materials from reliable and reputable sources:
The health certificate
or other documents issued by the exporting countries
should be checked; and
The documents must
be kept to maintain traceability.
Ensure optimal storage
conditions:
The freezing temperature
for foods should be at -18¢XC or below, and
the chilling temperature should be at 4¢XC or below; the temperature of the freezer or chiller should be monitored
regularly and proper record should be kept;
The raw ingredients
and prepared foods should be stored separately to
prevent cross-contamination;
After preparation and
during transportation and display, all sushi and sashimi
should be covered and kept at 4¢XC or below to reduce the risk of cross-contamination and
multiplication of bacteria; and
The leftovers should
be discarded after business hours.
Ensure the seafood is
used at its fresh state:
No excessive amount
of seafood should be stored; and
Apply ¡§First-in-first-out¡¨ principle
in stock keeping.
Observe
hygienic practice during food preparation and any
other handling process:
Hands should be properly
washed and direct touching of foods should be reduced
to a minimum ¡V use machines or wear disposable gloves;
All food handlers should
observe personal hygiene strictly;
Hygiene of the preparation
area and the equipment should be maintained in good
condition;
Utensils should be
cleaned and disinfected before and after use, separate
utensils should be used for the preparation of sushi
and sashimi; and
Sushi and sashimi should
be prepared in separate areas with good ventilation.
Advice on
hygienic practice can be found in the pamphlet titled
¡§Know more about Japanese Sashimi¡¨ and it can be obtained from the Food and Environmental
Hygiene Department.
Advice
to Consumers
Apart from
the trade, consumer is another important partner in contributing
to food safety in the public health sense. Sushi and sashimi
contain raw ingredients and exhibit distinct features
in the production process that are associated with increased
microbiological hazards, they are not advisable for people
with impaired immunity, including pregnant women, the
elderly, and those with chronic illness such as cancer.
For others who are generally healthy who wishes to consume
sushi and sashimi are advised to identify reliable and
reputable operators and choose the sushi and sashimi that
are in good conditions. The following are some clues for
these purposes.
1. Observe
the general hygiene of food premises
Common areas such as
the floor, wall and ceiling are clean;
Equipments such as refrigerators
for display of foods are clean and in good condition;
and
Utensils used to hold
the foods are clean and tidy.
2. Choose
sushi and sashimi that are in good conditions
Sushi and sashimi are
cold enough;
Rice of sushi is soft
and white;
Fish and shellfish should
look bright, glossy and transparent;
Fat of fish pieces, such
as salmon fillets, is clearly visible; and
FEHD
Microbiological Guidelines for Sushi and Sashimi
*
Unsatisfactory Hygienic Quality
a.
APC
(sushi, fish fillet & fish roe sashimi)
>
106 /g
APC
(sashimi other than fish fillet & fish
roe)
>
107 /g
b.
E.
coli (total)
>
104 /g
Note: For assessment of hygienic quality,
unsatisfactory means the results of APC are >
106/g for sushi, fish fillet &
fish roe sashimi, or > 107/g for
sashimi other fish fillet & fish roe, or the
results of E. coli (total) are > 104/g.
V. parahaemolyticus
is normally found in fish and shellfish. The organism
is likely to be part of the natural flora of fish caught
in coastal waters during the warmer months. Through contact
in the fish market, it can readily spread to deep-water
species and will multiply rapidly if the product is inadequately
chilled. It is a common cause of food poisoning in Japan
and in Hong Kong. Poisoning illness usually starts at
12 to 24 hours after ingestion, but the incubation period
may range from 2 hours to 4 days. Illness persists for
up to 8 days and is characterised by profuse watery diarrhoea
free from blood or mucus, abdominal pain, vomiting and
fever.
Salmonella
species.
Salmonellas
are one of the most important causes of food-borne illness
worldwide. Meat, milk, poultry, and eggs are primary vehicles
of this bacteria. Salmonella may be found in these primary
vehicles when they are undercooked, or in other foods
through cross contamination.
The
generally quoted infective dose is high at 100,000 cells
per gram. Other factors may include the virulence of the
serotype, the susceptibility of the individual and the
food vehicle involved. It causes an illness with nausea,
vomiting, abdominal cramps, diarrhoea, fever, and headache,
usually starting at 12 ¡V 36
hours after ingestion of the contaminated food.
Staphylococcus
aureus
S.
aureus is commonly found on hands, in throats, and nasal
passages of humans. It is introduced to the food through
improper handling. The storage temperature and duration
are most important contributing factors to the multiplication
of this organism. When it is ingested in large doses,
at the range of 100,000 per gram, Staphylococcal food
poisoning may occur. It generally occurs in two to four
hours after ingestion. The disease course is relatively
mild and short-lived. Nausea, vomiting, stomach cramps,
retching and prostration are the predominant symptoms,
although diarrhoea is also often reported, and recovery
is normally complete within 1-2 days.
Listeria
monocytogenes
L.
monocytogenes is the only important human pathogen among
the seven species currently recognized within the genus
Listeria. L. monocytogenes will grow over a wide range
of temperature from 0-42¢XC with an optimum between
30 and 35¢XC.
L. monocytogenes is normally found in milk products, vegetables,
poultry and meat. It could be introduced to fish and shellfish
by cross-contamination by other food items.
The
incubation periods for the disease is typically a few
weeks, but may range from one to 90 days. Symptoms of
the disease, which is most likely to develop in pregnant
women, the very young or elderly and the immunocompromised,
can vary from a mild, flu-like illness to meningitis and
meningoencephalitis. In pregnant women, the symptoms are
generally mild with fever, gastrointestinal upset, or
flu-like symptoms. The main impact is on the foetus or
newborn which can be fatal.
References:
Adams MR &
Moss MO Bacterial agents of foodborne illness. In: Food
Microbiology. England. Cambridge: The Royal Society
of Chemistry; 1995.
International
Commission on Microbiological Specifications for Foods.
Micro-organisms in Foods 5. London: Blackie Academic
& Professional; 1996.
Benenson AS,
editor. Control of Communicable Diseases Manual. Sixteenth
Edition. Washington DC: American Public Health Association;
1995.
Under
Schedule 2 to the Food Business Regulation (subsidiary
legislation of Cap. 132), sashimi and sushi are classified
as restricted foods (items 18 and 19 respectively of the
Schedule).
2.
The sale of restricted foods including sashimi and sushi
is governed by section 30(1)(a) of the same Regulation
as follows:
¡§30.
Restriction on the sale, etc. of articles specified
in Schedule 2
(1)
Save with the permission in writing of the Director,
no person shall ¡V
sell
or offer or expose for sale, or possess for
sale or for use in the preparation of any
article of food for sale, any of the foods
specified in items 1 to 5 inclusive, items
9 to 14 inclusive and items 16 to 20 inclusive
of Schedule 2:
Provided
that this paragraph shall not apply to the hawking
of live poultry in any place or area for the
time being set aside by the Director pursuant
to section 4(1)(a) of the Hawker Regulation;¡¨
3.
Thus any person who wishes to sell or prepare for sale
sashimi and sushi must apply for appropriate licence or
permit from the Director of Food and Environmental Hygiene.
4.
With effect from 1 March 1997, all premises engaged in
the preparation and sale of ¡§sushi¡¨ and ¡§sashimi¡¨
are subject to one of the following
means of licensing control:
a general restaurant
licence with specific endorsement is required when these
food items are prepared, handled and sold for consumption
on the premises;
a food factory
licence with specific endorsement is required when these
food items are prepared, handled and sold for consumption
off the premises; and
a restricted
food permit is required for only selling these food
items for consumption off the premises, such as from
a licensed fresh provision shop. The food has to be
supplied from a source approved by the Director.
This
is a publication of the Food and Public Health Branch
of the Food and Environmental Hygiene Department of HKSAR
Government. Under no circumstances should the research
data contained herein be reproduced, reviewed, or abstracted
in part or in whole, or in conjunction with other publications
or research work unless a written permission is obtained
from the Department. Acknowledgement is required if other
parts of this publication are used.
Correspondence:
Risk
Assessment Section
Food and Environmental Hygiene Department
43/F, Queensway Government Offices,
66 Queensway, Hong Kong.
Email:enquiries@fehd.gov.hk