Foodborne Botulism Regional Variation

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The global epidemiology of foodborne botulism has been shaped by regional diet and soil ecology. Perhaps any food can cause botulism if it is contaminated with a neurotoxigenic clostridium, processed and stored under permissive conditions, and undercooked before consumption. Despite this potential, a majority of botulism is caused by a minority of foods (Table 3), reflecting in any region those culturally preferred foods in which botulinum neurotoxin is produced and persists. Similarly, a single neurotoxin type causes most foodborne botulism in a given region, usually the predominant type capable of causing human botulism found in that region's soil. Hauschild (8) and Dodds (62) have compiled comprehensive global reviews of the epidemiology of botulism and the soil microbiology of C. botulinum.

The etymology of botulism may be more apparent in its Polish translation, kielbasianym, as it is arguable that more people have eaten a kielbasa, or polish sausage, than know that the ancient Romans called their sausages botuli. Of any nation, the most foodborne botulism is diagnosed in Poland due to the contamination of home-canned pork, ham, and sausage with type B toxin. From 1988 to 1992 there was a median of 314 cases per year of foodborne botulism reported in Poland (63) compared to 24 cases in the United States (64). The remainder of Central and Eastern Europe

TABLE 3 Patterns in Global Epidemiology of Foodborne Botulism

Predominant neurotoxin type

Predominant contaminated food

Americas

Canada, Alaska Continental United States.

Fermented fish and aquatic mammals

Western

Vegetables and fruits Vegetables and fruits Vegetables and fruits

Eastern Argentina

Eurasia

Scandinavia

Central and eastern Europe

Poland

Italy, Spain

Iran

Fomer Soviet Union

Fish and aquatic mammals Meat

Vegetables and fruits

Fish eggs

Fish

Ham, mushrooms Fermented soy beans Fermented fish

China Japan

shares a predominance of type B botulism due to meat products (8). While type B is also the most common type of foodborne botulism in Italy and Spain, the implicated foods in these southern European countries are usually home-canned vegetables and capsicums (peppers) (7,8).

Vegetables and fruits also are the most frequent vehicle of foodborne botulism in the continental United States, with the toxin type varying by region. Of laboratory-confirmed outbreaks of foodborne botulism in the United States from 1899 to 1989, 57 (69%) of 83 due to type B neurotoxin occurred east of the 95th meridian, while 254 (86%) of 297 due to type A occurred to the west (54,64). In his systematic soil survey, Smith (65) found 73% of type B isolates from soils collected in the eastern United States and 88% of type A isolates from the western United States, corroborating earlier results of Meyer and Dubovsky (66). Although produce prepared at home has caused most outbreaks of botulism in the United States, recent outbreaks due to foods prepared in restaurants have accounted for a disproportionately large number of cases (6).

In the Americas south of the United States, almost all reports of foodborne botulism have originated from Argentina, where 70 outbreaks were noted from 1922 to 1997 (67). The epidemiology in Argentina is similar to the western United States. Home-canned fruits and vegetables have caused most outbreaks. All but six laboratory-confirmed outbreaks through 1997 were caused exclusively by type A toxin. Over 70% of typable neurotoxigenic strains isolated in Argentina produced type A toxin (68).

From 1958 to 1989, a mean of 90 foodborne botulism cases was diagnosed each year in China (69). Fermented legumes, usually strong-smelling soybean curd (chou-doufu), caused over 60% of these cases. Over 75% of typed cases were due to type A neurotoxin, and 80% were diagnosed in a single northwestern province, where type A C. botulinum was the most prevalent neurotoxigenic clostridium isolated in the soil.

Type E C. botulinum has been cultured from a variety of aquatic sediments and inhabitants. It has been the predominant type isolated in Canada and Alaska, found in up to 74% of coastal soil samples (70). Type E botulism in humans has a strong association with the consumption of fermented fish and aquatic animals. Type E toxin consumed in aquatic foods caused 81% of foodborne botulism outbreaks in Alaska through 1989 (54,64) and 97% of outbreaks in Canada from 1994 to 1997 (71). Type E is also the most frequent type of foodborne botulism in Japan (72), Iran (73), and Scandinavia (8). To reiterate, the specific foods associated with type E botulism reflect regional cuisine. For the native peoples of Canada and Alaska, frequent vehicles are fermented seal, whale, and the eggs and heads of salmon (74). In Japan, two related fermented fish dishes, izushi and kirikomi, have caused nearly all reported cases (8). Other vehicles have been salt-cured fish and fish eggs in Iran, seal meat in Greenland, and herring and half-fermented trout (rakfisk) in continental Scandinavia.

Cervelas, thick pork sausage akin to mortadella, caused an outbreak of 60 cases of type E botulism in Madagascar (75), while ham caused smaller outbreaks in France (8), the former Soviet Union (76), and Argentina (77). Type E botulism due to neurotoxigenic C. butyricum was first described in Italian infant botulism cases (24), for whom the source of spores was not identified. An outbreak of type E botulism in eastern China in 1994 was caused by a paste of fermented soybeans and winter melon contaminated with C. butyricum (12,78). Investigation of this outbreak led to the discovery that two prior outbreaks in China of type E botulism due to fermented soybeans were caused by C. butyricum (12). Gram (legume) flour was the source of toxigenic C. butyricum implicated in a 1996 outbreak of botulism in India (13). The only type E botulism outbreak in the United States not associated with aquatic foods occurred in California in 1941 (79). Botulism was caused by toxic imported Yugoslavian mushrooms, from which no organism was ever cultured. Could these cases have been caused by C. butyricum, subsequently identified as an agent of botulism in Italy, located across the Adriatic Sea from Yugoslavia? Routine microbial procedures at that time may not have been capable of detecting the lipase-negative C. butyricum as a source of neurotoxin. In any outbreak of type E botulism where the suspected food contains a vegetable or fruit grown in Eurasia, care should be taken to search for toxigenic C. butyricum.

Cases of foodborne botulism from type F C. botulinum, while very rare, have been caused by liver paste in Denmark (80), venison jerky in California (81) and pickled cucumbers in Argentina (67). In some regions there is a seasonal occurrence of foodborne botulism reflecting those months when home-preserved foods are consumed more frequently (8).

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