Introduction
What is botulism?
Clostridium Botulinum in fish
Outbreaks originating from hot-smoked fish
The possible danger in the UK
Time taken in days for experimentally inoculated products to become toxic
Smoked fish and botulism
How to control botulism
Summary
Fish in the UK is one of the safest articles of diet; statistics for food poisoning make this quite clear. But several cases of botulism have occurred in other countries in recent years, and investigations have shown that it could happen here.
The likelihood of such an outbreak occurring is remote, but there is no room for complacency; one isolated incident could do irreparable harm to the fish industry as a whole.
This note explains the cause of botulism, describes how outbreaks abroad have happened, and gives advice to producer and consumer on how the hazard can be averted.
Botulism is an often fatal food poisoning disease caused by one of the most powerful toxins known to man. A toxin is a poison produced by certain bacteria when they grow on food; the kind of bacterium that forms the toxin causing botulism is called Clostridium botulinum. When food containing the toxin is eaten, the nervous system is affected and death can follow within hours.
There are seven known types of Clostridium botulinum, referred to as types A-G; of these, A, B, E and F consistently produce botulism in humans, and B, E and F are frequently found in the sea.
Authentic cases of botulism have been recorded in recent years in places as far apart as Japan, Scandinavia and North America. Since these have been due mainly to type E, usually in association with the eating of seafoods of various kinds, worldwide attention has been given to the occurrence of type E in fish and fishery products.
Clostridium botulinum grows only in the absence of oxygen, and type E, and some varieties of B and F, have two important properties. First, they are found in fish intestines and gills and in mud from the sea, whereas the other types are found mostly in soil. Secondly, they grow and form toxin at a much lower temperature than the other types; they can grow at 5°C in fish products. Fortunately the toxin is readily destroyed by cooking since it does not survive exposure to 70°C for 2 minutes.
Outbreaks of botulism associated with the eating of hot-smoked fish in North America in the 1960s were at first thought to be directly attributable to vacuum packing. Consequently Canada banned the import of all types of packaged fish, and in particular kippers. This restriction was later lifted when fuller investigation indicated that the most probable cause was the change that had gradually taken place in the traditional process of hot smoking, and that vacuum packing itself caused little increase in toxin production.
Over the years public taste has changed and with it the methods of curing. At one time the product was so heavily salted, smoked and dried that Clostridium botulinum, where present in fish, could not grow and produce toxin. Such a heavily cured product needed to be neither refrigerated nor vacuum packed during distribution. Nowadays hot-smoked fish are distributed with much less smoke and salt, and much more moisture, with the result that any Clostridium botulinum present can more readily form toxin when the fish are kept warm for some length of time.
Moreover, vacuum packing extends the shelf life of the lightly smoked product by suppressing the growth of other bacteria and moulds, thus allowing any type E present an even longer time than before in which to flourish and produce the poison; increase in the amount of toxin present is not necessarily accompanied by sufficient deterioration in quality of the product to put people off eating it. Infected hot-smoked fish not packed under vacuum can also become toxic when kept for a long period at too high a temperature.
When the sources of the North American outbreaks were examined, type E was found in the raw fish, in the mud from the bottom of the lake in which the fish were caught, in the curing premises and in the finished product; it is perhaps surprising that many more cases of botulism than those recorded had not occurred.
Although the North American outbreaks of botulism caused concern, of more direct consequence to the UK fish industry was an outbreak of type E botulism in Germany in 1970 caused by smoked trout from a fish farm. Although this was an isolated incident involving only 3 people, the market for Danish and British farmed trout was seriously affected for a time.
The important lesson to be learnt from these outbreaks is that a change in established practice can result in a change in the way the product spoils, and can encourage growth of food poisoning organisms accompanied by production of their toxins. Consequently any change in processing method should always be followed by careful bacteriological examination of the product under various conditions of handling and storage.
Outbreaks of botulism in the UK are rare; the last recorded case was in 1955 due to the consumption of a pickled product made from imported fish. Why is it then that Britain has remained relatively free of botulism when, during the same period, several outbreaks have occurred in neighbouring countries from which we import fish? The reason is twofold. First, the incidence of Clostridium botulinum is low in the seas from which the UK traditionally takes its fish and, secondly, the fish are usually cooked and eaten on the same day. Raw, pickled or fermented fish products that have often been the cause of outbreaks of botulism on the Continent are not eaten to any great extent in the UK. The incidence of organisms that cause botulism is high in the waters of the Baltic, the Kattegat and the Skagerrak, but is far less in the English Channel, the North Sea, the Irish Sea and the Minches of NW Scotland. Nevertheless the organism has been isolated from herring, sprats, mackerel and turbot caught in British waters.
The organism is found to some extent in trout farmed in fresh water, not unnaturally since Clostridium botulinum is found in soil. Contamination of farmed trout in the UK varies from 0 to 100 per cent depending on the kind and location of the farm; the organism can be present in the water and mud in an affected pond, on fish eggs and in the intestines and gills offish.
Tests on 646 samples of vacuum packed fish on sale in British shops as far apart as Aberdeen and Bristol, Liverpool and Hull, showed that toxin developed in 5 packages after improper storage. This survey thus showed that the organism does occur in UK fish but that the incidence is low.
Following this survey, a number of different fish products in vacuum packs were inoculated with type E to find out whether toxin would be produced, and if so how quickly, at various temperatures of storage. The results of these tests are shown in the table.
|
Fish product |
Temperature of storage |
||
|
|
5°C |
10°C |
20°C |
|
Herring |
11 |
5 |
1 |
|
Cod |
negative |
10 |
|
|
Plaice |
negative |
10 |
|
|
Scallops |
|
negative |
6 |
|
Kippers |
negative |
9 |
2 |
|
Smoked salmon |
negative |
18 |
7 |
|
Smoked trout |
|
11 |
5 |
|
Smoked haddock |
|
29 |
3 |
Three things are apparent from these results. First, the higher the temperature of storage, the faster the organisms multiply and form toxin. Secondly, toxin is formed more slowly in smoked fish than in wet fish, and thirdly, the fish can become toxic within the keeping time of the product.
Since most of the packs examined contained products that would be cooked before being eaten, any toxin already formed would be destroyed; such products could therefore be assumed to be safe.
Some products however are eaten either raw or without further cooking; smoked salmon, smoked trout and smoked mackerel are the most common examples.
Many of the salmon and trout that are smoked in this country are imported from Japan, Denmark and the Pacific coast of North America. Clostridium botulinum type E has been found in all these areas of the world. Moreover, sliced smoked salmon is sold in quantity in vacuum packs.
Salmon flesh is either dry salted or brined before being cold
smoked, the time of salting varying with the size of salmon being cured. The
presence of salt in the product has a great effect on the growth of
Clostridium botulinum, but the concentration of salt in smoked salmon is
not usually high enough to prevent growth altogether; commercial smoked salmon
usually contains 1 to 4 per cent salt. The concentration required to prevent
growth at room temperature can vary from as low as
3
per cent to 5 per cent or
more, so that the amount of salt present in smoked salmon is on its own no
guarantee against the danger of botulism.
Trout and mackerel are brined and then hot smoked, either as gutted whole fish or as fillets. The range of salt concentration is similar to that found in salmon. Details of the smoking process for salmon, mackerel and trout are given in Advisory Notes 5, 66 and 74 respectively. Since neither the smoking nor the drying parts of present processes are particularly severe, Clostridium botulinum can survive and flourish in the finished product, unless it is kept sufficiently cool.
Before the toxin of Clostridium botulinum can develop in a fishery product a number of factors must coincide: the organism must be present in the fish, the time and temperature of storage must be favourable for toxin production, and the chemical composition of the product must be such that it supports the growth of the organism. Elimination of any one of these factors will make the product safe.
In practice it is not possible to rid a contaminated fish of botulinum organisms but removal of the guts and gills, followed by thorough washing of the belly cavity with tap water, can reduce contamination by as much as 90 per cent.
Starvation of farmed trout for 1-3 days before harvesting is beneficial as fish with empty guts cause less contamination during processing. For this procedure to be effective, however, the starved fish should be held in concrete or plastics ponds; hungry trout in dirt ponds will feed off the contaminated mud.
Clostridium botulinum types B, E and F can grow and produce toxin at 5°C in some fish products; the lowest recorded temperature for growth in any food is 3·3°C, when the product took 31 days to become toxic. In practice, therefore, if fish are adequately iced immediately after catching and kept below 4°C at all stages of processing until eaten, they will remain safe.
Caterers and retailers receiving deliveries of fresh fish must inspect and where necessary re-ice them to maintain the temperature of the fish below 4°C. Where the amount of ice on receipt is insufficient, the supplier should be notified. A chillroom operating at 4°C can be used to conserve ice around fish but cannot be used satisfactorily to cool uniced fish or keep them cool. Packaged fish should carry a ‘Sell by.........’ date according to the type of product, clearly marked ‘Store below 4°C’ and carry a recommendation that the contents be eaten within 24 hours if kept at room temperature and within 3 days if kept in a refrigerator. Fish presented for sale without refrigeration should be discarded if unsold at the end of a day’s trading.
Alteration of the chemical and microbiological composition offish by the addition of enough salt or acetic acid can make the fish completely safe but the high concentration required would not be acceptable to most consumers. However, a pH level of 4·5 in marinated products or a salt concentration of 3·0 per cent in smoked fish products is usually acceptable and affords added protection and extension of refrigerated shelf life.
1. The risk of an outbreak of botulism from eating fish products in this country is remote but is nevertheless present.
2. The bacterium that produces the toxin, Clostridium botulinum, has been found in British fish and in coastal and inland waters, and is certainly present in other areas of the world from which fish are imported to the UK.
3. The bacterium can grow at a temperature as low as 3·3°C but its toxin is destroyed by heating it at 70°C; any product that is properly cooked and eaten the same day is therefore safe; the main danger lies in products that either can be eaten raw, such as smoked salmon, or need not be cooked by the consumer, for example hot-smoked fish.
4. Changes in traditional method of processing can introduce new hazards; for example, reduction in the amount of salt or smoke can allow the bacterium to flourish, or the use of vacuum packs can extend the shelf life of the product sufficiently to allow the product to become toxic during storage.
5. Smoked salmon and hot-smoked trout and mackerel are the products most likely to give trouble in the UK. All such products should have a minimum concentration of 3 per cent salt.
6. The safety of any product is assured if the fish are stored
at a chill temperature below 4°C from the time they are caught until they
are eaten.
