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International Notes Type B Botulism Associated with Roasted Eggplant in Oil -- Italy, 1993

In August and October 1993, public health officials in Italy were notified of seven cases of type B botulism from two apparently unrelated outbreaks in different communites. Investigations were initiated by the Regional Health Observatory of Campania and the Italian National Institute of Health. This report summarizes the outbreak investigations, which indicated that illness was associated with eating commercially prepared roasted eggplant in oil. Outbreak 1

On August 14, two waitresses working in a sandwich bar in Santa Maria di Castellabate were admitted to a local hospital with dysphagia, diplopia, and constipation; a clinical diagnosis of botulism was made. On August 12, the waitresses had prepared and eaten ham, cheese, and eggplant sandwiches. A third waitress also ate the sandwiches and developed dyspepsia for which vomiting was induced; she did not have neurologic symptoms. The owner of the bar, who had tasted a small piece of eggplant from the same jar later on August 12, remained asymptomatic. The cook had initially opened the jar of commercially prepared sliced roasted eggplant in oil and had tasted its contents on August 11 and developed diarrhea. Both the cook and the owner reported that the eggplant tasted spoiled.

Botulism was presumptively diagnosed in the two hospitalized patients; both were treated with trivalent botulism antitoxin and gradually improved. No food samples were available for testing. No botulism toxin was detected in the serum of the two hospitalized patients. However, cultures of their stools subsequently yielded type B Clostridium botulinum. Outbreak 2

During October 5-6, four of nine members of an extended family who had dined together on October 2 were hospitalized in Naples with suspected botulism. The meal consisted of green olives, prosciutto, bean salad, green salad, mozzarella cheese, sausages, and commercially prepared roasted eggplant in oil. Based on an investigation and analysis of food histories, the eggplant was implicated as the probable source (relative risk=undefined; p less than 0.01). All of the patients were treated with trivalent botulism antitoxin and gradually improved. Investigation indicated that on September 27, another family member had opened and dipped a fork into the implicated jar of eggplant; although he did not eat any eggplant, he used the fork for other food items. On September 28, he had developed vomiting, dysphagia, and double vision but was not hospitalized; his symptoms resolved spontaneously. On October 8, he was asymptomatic but was hospitalized and treated with trivalent botulism antitoxin after botulism was diagnosed in other family members.

One of the hospitalized patients developed respiratory muscle weakness and required mechanical ventilation. A serum specimen from one patient was negative for botulism toxin. Cultures of stool specimens from three patients yielded proteolytic type B C. botulinum. No eggplant was available for testing. Follow-Up

The commercially prepared eggplant suspected of causing both outbreaks was produced by one company and sold only in Italy. The company reported preparing the eggplant in the following manner: eggplant slices were washed and soaked overnight in a solution of water, vinegar, and salt; roasted in an oven; and subsequently placed in glass jars. Garlic, peppers, oregano, and citric acid were added. The mixtures then were covered with sunflower oil and sealed with screw-on lids; after being filled, the jars were boiled in water for 30 minutes. The pH of the product was not consistently monitored. A total of 119 jars of eggplant from the same lot that caused the outbreaks was tested; neither C. botulinum spores nor botulism toxin were detected. The pH of the product varied from 3.9 to 5.1; the pH was greater than 4.6 in 24 (20%) jars tested.

Public health officials issued a national warning and recalled unused jars of eggplant. No additional cases of botulism associated with this product were reported. Reported by: P D'Argenio, MD, F Palumbo, MD, R Ortolani, MD, R Pizzuti, MD, M Russo, DBiol, Regional Health Observatory of Campania, R Carducci, MD, Cardarelli Hospital, M Soscia, MD, Contugno Hospital, Naples; P Aureli, DBiol, L Fenicia, DBiol, G Franciosa, DBiol, National Institute of Health, Rome; A Parella, MD, Public Health Dept, Eboli; V Scala, MD, Public Health Dept, Vallo della Lucania, Italy. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; Global EIS Program, International Br, Div of Field Epidemiology, Epidemiology Program Office, CDC.

Editorial Note

Editorial Note: Foodborne botulism is a paralytic illness caused by the ingestion of botulism toxin, a neurotoxin produced by the ubiquitous spore-forming bacterium C. botulinum. Although botulism toxin in food can be destroyed by heating to boiling (212 F {100 C}) for 10 minutes, the spores are heat resistant and can survive prolonged boiling. To destroy C. botulinum spores, food must be heated under pressure to temperatures substantially greater than 212 F. Certain environmental conditions, such as absence of oxygen (anaerobic conditions), pH greater than 4.6, warm temperatures (generally greater than 39 F { greater than 4 C}), high moisture content (water activity), and lack of competing bacterial flora promote production of botulism toxin in foods contaminated with C. botulinum spores. The process used to produce the eggplant epidemiologically implicated in the outbreaks in Italy probably failed to remove C. botulinum spores and may have provided such conditions.

Covering foods in oil may provide the anaerobic conditions required for the production of botulism toxin. Outbreaks of botulism in the United States and Canada have been caused by covering vegetables with oil or grease. For example, in 1983, onions covered in grease and left overnight on a grill caused a large outbreak of botulism in Illinois (1), and commercially processed garlic in oil caused outbreaks in 1985 and 1989 (2,3). As a result of these outbreaks, the Food and Drug Administration recommended the addition of antimicrobial growth inhibitors or acidifying agents to such products (4).

In Italy, approximately 50 cases of botulism are reported annually (National Institute of Statistics, unpublished data, 1994), compared with approximately 20 cases annually in the United States (CDC, unpublished data, 1994). However, because the clinical and laboratory diagnoses of botulism can be difficult, these counts of incident cases probably underestimate the actual occurrence. In the United States, surveillance for botulism is linked to the release of botulism antitoxin for treatment of suspected cases. CDC maintains supplies of botulism antitoxin at quarantine stations nationwide for rapid release at the request of state health officials who report suspected cases. This centralized system for controlling antitoxin supplies results in reporting of botulism cases and a well-maintained, reliable source of antitoxin; no such system exists in Europe.

In Italy, as in the United States, outbreaks of botulism associated with commercial products are uncommon; most result from eating improperly preserved home-canned foods (National Institute of Statistics, unpublished data, 1994). However, two previous outbreaks in Italy have been linked to commercial products -- mushrooms in oil and pickled olives (5). The outbreaks described in this report probably resulted from a commercial process that was inadequate to prevent contamination of the final product with C. botulinum spores. Another potential explanation is that the jars of eggplant may have been contaminated after they were opened; however, this is less likely because both outbreaks were caused by the same commercial product. Once contaminated with spores, the pH, oil covering, and lack of refrigeration probably provided conditions conducive to the production of botulism toxin. Strict control of the commercial processes used to manufacture such products and the addition of antimicrobial growth inhibitors or acidifying agents could assist in preventing such outbreaks. Persons who prepare roasted vegetables in oil at home should be aware that this practice may be hazardous, especially if such foods are allowed to remain above refrigerator temperature (generally greater than 39 F { greater than 4 C}).

References

  1. MacDonald KL, Spengler RF, Hatheway CL, Hargrett NT, Cohen ML. Type A botulism from sauteed onions: clinical and epidemiologic observations. JAMA 1985;253:1275-8.

  2. St. Louis ME, Shaun HS, Peck MB. Botulism from chopped garlic: delayed recognition of a major outbreak. Ann Intern Med 1988;108:363-8.

  3. Morse DL, Pickard LK, Guzewich JJ, Devine BD, Shayegani M. Garlic-in-oil associated botulism: episode leads to product modification. Am J Public Health 1990;80:1372-3.

  4. Food and Drug Administration. Press release no. P89-20. Washington, DC: US Department of Health and Human Services, Public Health Service, Food and Drug Administration, April 17, 1989.

  5. Fenicia L, Ferrini AM, Aureli P, Padovan MT. Epidemic of botulism caused by black olives {Italian}. Industrie Alimentari 1992;31:307-8.




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