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From the Centers for Disease Control and Prevention
March 15, 2006

Multiple Outbreaks of Gastrointestinal Illness Among School Children Associated with Consumption of Flour Tortillas—Massachusetts, 2003-2004

JAMA. 2006;295(11):1244-1246. doi:10.1001/jama.295.11.1244

MMWR. 2006;55:8-11

Ten outbreaks of gastrointestinal illness among school children at nine different schools were reported during February 2003–May 2004 to the Massachusetts Department of Public Health (MDPH). These outbreaks occurred among children who ate lunch provided by the schools and were characterized by short incubation periods and short durations of illness. The clinical and epidemiologic characteristics of the outbreaks were similar to those of previously reported outbreaks of vomiting associated with burritos served at multiple schools in the United States in 1997-1998.1,2 Epidemiologic investigation of the 1997-1998 outbreaks implicated burritos made with flour tortillas as the suspect vehicle; no etiologic agent was identified, but symptoms suggested either a biotoxin or chemical agent. This report describes epidemiologic and laboratory findings from three of the 10 outbreaks in Massachusetts. Consumption of flour tortillas from a single manufacturer was significantly associated with illness. Preliminary results indicated elevated levels, relative to common industry practices, of potassium bromate and calcium propionate in the implicated tortillas. School officials should be aware of the need for rapid action during outbreaks with short incubation periods and short durations and should notify local and state health officials immediately to ensure rapid response and collection of epidemiologic information, clinical specimens, and food samples.

Middlesex and Suffolk Counties, September 2003

In September 2003, MDPH received a report that multiple students sought medical attention from the school nurse after eating lunch at school A. The lunch was prepared by a caterer and served at three schools that day. Ill students were identified at two of the three schools (schools A and B). An investigation was conducted among 59 students in grades 6-7 from school A and 63 students in grades 5-6 from school B. Illness was defined as having at least one gastrointestinal symptom (nausea, vomiting, abdominal cramps, or diarrhea) and one neurologic symptom (headache, dizziness, tingling, or burning in mouth) within 24 hours of lunch consumption. Predominant symptoms at school A were headache (87%), nausea (80%), abdominal cramps (67%), and dizziness (53%) and at school B were abdominal cramps (88%), nausea (69%), headache (69%), and dizziness (69%). Each student was administered a questionnaire about consumption of items from the school lunch menu. The menu included chicken fajitas served with flour tortillas.

Fifteen (25%) of 59 students surveyed at school A and 16 (25%) of 63 students surveyed at school B became ill after eating the lunch. Median onset of illness was 14 minutes (range: 1-330 minutes) after lunch consumption at school B and 35 minutes (range: 5-1,440 minutes) at school A. Median duration of illness ranged from 5 hours (school B; range: 1-96 hours) to 7 hours (school A; range: 1-72 hours). At school A, univariate analyses identified the flour tortilla component of the chicken fajita as the only food item associated with illness (100% of ill students reported having eaten tortillas; relative risk [RR] = 6.6; p = 0.05). At school B, univariate analyses identified the flour tortilla component of the chicken fajita as the only food item significantly associated with illness (94% of ill students reported having eaten tortillas; RR = 6.5; p = 0.02). A positive dose-response relationship was noted with consumption of the chicken fajita (Mantel-Haenszel chi-square = 8.14, p = 0.004) at school B (i.e., the more chicken fajita the child ate, the more likely the child was to become ill). The flour tortillas used in the chicken fajitas at schools A and B were traced to Manufacturer A in Chicago, Illinois.

Suffolk County, May 2004

In May 2004, MDPH investigated an outbreak of gastrointestinal illness among students who ate lunch at school C. An investigation was performed among 187 students in grades 1-6. Illness was defined as at least one gastrointestinal symptom (nausea, vomiting, abdominal cramps, or diarrhea) and one neurologic symptom (headache, dizziness, tingling, or burning in mouth) within 24 hours of consuming the meal. The predominant symptoms were nausea (89%), headache (83%), abdominal cramps (61%), fatigue (56%), dizziness (47%), and vomiting (42%). Students in grade 1 and grades 3-6 were interviewed by MDPH epidemiologists using pictures of food items served for lunch. The menu included chicken fajitas served with flour tortillas.

Thirty-six (19%) of 187 students surveyed at school C became ill after eating the lunch. Forty-nine percent of the ill students reported symptom onset within 30 minutes of consuming lunch. Univariate analyses identified both chicken fajita with flour tortilla (47% of ill students reported having eaten tortillas; RR = 3.1; 95% confidence interval [CI] = 1.8-5.2) and orange juice (19% of ill students reported having consumed orange juice; RR = 2.4; CI = 1.3-4.3) as food items significantly associated with illness. Traceback of the flour tortillas identified manufacturer A as the source.

Environmental Findings

The Massachusetts Food Protection Program, in cooperation with local boards of health and the New England District Office of the Food and Drug Administration (FDA), conducted environmental investigations and tracebacks of ingredients used in the implicated foods for each school food-service operation. No contributing factors at the food preparation or serving sites were identified. Labels and invoices were obtained during the tracebacks of foods and ingredients used in the school lunches that triggered the outbreaks. The only common food source identified was manufacturer A, which produced all of the tortillas implicated in the outbreaks. Schools received the commercially packaged tortillas under refrigeration, in different sizes, under various brand names, from three distributors in Massachusetts and Connecticut. The packaged tortillas were kept under refrigeration until use and did not undergo further processing at the schools.

In October 2003, staff from the regional office of the Chicago District Office of FDA, the Illinois Department of Public Health, the Chicago Department of Public Health, and CDC inspected the facilities of manufacturer A. FDA noted several deficiencies at the plant, including improper storage, use, and labeling of chemicals; food ingredients and additives in unlabeled containers; food contact surfaces not protected from environmental contamination; and a lack of backflow protection from a piping system that discharged waste water. Limited recordkeeping impeded verification of employee practices and history relating to cleaning and maintenance of equipment. Tortilla packages were inconsistently marked with a manufacturing code date based on a 45-60 day shelf-life. The recipe for the product was obtained; calcium propionate and bromated flour were among the ingredients listed. FDA collected and analyzed samples of ingredients and finished products.

Laboratory Findings

Tortilla samples from schools A, B, and C submitted to FDA tested negative for heavy metals, T-2 toxin, deoxynivalenol, aflatoxins, amanitin, ricin, mold, yeast, staphylococcal enterotoxins, and both Bacillus cereus diarrheal (heat labile) and emetic (heat stable) enterotoxins. Unopened tortilla samples collected from one school, manufacturer A, and local retail outlets were evaluated for potential toxicity using a sequential solvent extraction and separation scheme, with each fraction subjected to a toxicologic screening using Bacillus megaterium (ATTC 25848) and brine shrimp (Artemia spp). Preliminary results indicated low toxicity in organic fractions and high toxicity in acid-base and enzymic-digestion fractions of both outbreak and control tortillas. Substantial levels of the food-processing additives calcium propionate (2%-3%, five to 10 times the expected amount, based on common industry practices) and potassium bromate (1-2 mg/kg, more than 50 times the level normally found in loaf breads, but similar to levels occasionally detected in buns and rolls) were found in the outbreak samples. Elevated levels of calcium propionate and potassium bromate were not identified in the control samples obtained from local retail stores.

Urine specimens were collected from five ill students from school A within 24 hours of the suspect meal and again 1 week later and submitted to the National Center for Environmental Health at CDC. Urine specimens were negative for alkylphenols (representing exposure to surfactants found in cleaning products) and bromides.

Reported by:

T LaPorte, MS, G Conidi, MPH, D Heisey-Grove, MPH, P Gadam, MPH, S Soliva, MPH, P Neves, A DeMaria, MD, Massachusetts Dept of Public Health. N Fico, Joint Institute for Food Safety and Applied Nutrition, College Park, Maryland. S Trujillo, PhD, H Njapau, PhD, CR Warner, PhD, BJ Canas, RM Eppley, PhD, EAE Garber, PhD, ME Stack, MS, VH Tournas, PhD, DL Park, PhD, FDA. H Schurz Rogers, PhD, M Patel, MD, J Osterloh, MD, AM Calafat, PhD, National Center for Environmental Health; A Fry, MD, A Bowen, MD, A DuBois, MD, National Center for Infectious Diseases, CDC.

CDC Editorial Note:

The outbreaks described in this report were characterized by short incubation periods and short durations of illness, with headache, nausea, abdominal cramps, and dizziness as predominant symptoms. These outbreaks were similar to previously reported outbreaks of vomiting associated with burritos served in lunches at schools in the United States in 1997-1998.1,2 The clinical characteristics reported in all of these outbreaks are consistent with exposure to an as yet unidentified pre-formed toxin or chemical agent. In such outbreaks, rapidly obtaining epidemiologic data and clinical and food samples is essential to determining illness etiology. School officials should be aware that illness outbreaks of short incubation involving neurologic and gastrointestinal symptoms might have resulted from chemical ingestion and should contact public health authorities immediately when this syndrome is observed. Health officials should obtain food samples for testing and, when possible, obtain urine specimens from ill and well children within 24 hours of exposure.

In addition to the three outbreaks described in this report, seven similar outbreaks occurred in Massachusetts during February 2003–May 2004. Flour tortillas were served before all seven outbreaks; manufacturer A was the source of the flour tortillas in six outbreaks. The last reported outbreak was in Suffolk County in May 2004.

Further chemical analyses are necessary to determine the cause of these outbreaks. Testing by FDA did not reveal Bacillus cereus diarrheal or emetic toxin, gastrointestinal mushroom toxins, or other biotoxins. Certain biotoxins, such as staphylococcal and clostridial enterotoxins, are unlikely to occur in association with tortillas; submitted specimens tested negative for these toxins. No heavy metals or seafood toxins were identified in the school lunches. Several other chemicals were considered as possible causes of the outbreaks, including unlabeled cleaning agents used in the factory. Although detergent contamination of the food was possible, the absence of urinary alkyl phenols reduces the likelihood that such contamination occurred.

Testing did reveal elevated levels of calcium propionate and potassium bromate in the implicated tortillas. However, these findings do not establish that potassium bromate and calcium propionate were factors in the etiology of these outbreaks. Calcium propionate has long been used in bakery products as a mold inhibitor and is generally regarded as safe for ingestion at low levels; however, ingestion of larger-than-usual amounts (based on common industry practices) might decrease the gastric emptying rate and cause gastrointestinal irritation, especially in younger children.3 Potassium bromate is used as a flour improver to strengthen dough and enable higher rising. Under proper baking conditions, potassium bromate levels are <20 μg/kg in finished bread products. However, if too much potassium bromate is added, or if the product is not cooked long enough or at adequate temperatures (tortillas are baked for a short period of time at temperatures lower than other baking products), more residual additive might remain. Foods contaminated with much higher levels of potassium bromate can cause acute irritation to the gastrointestinal tract, resulting in nausea, vomiting, abdominal pain, and diarrhea; poisoning episodes in children involving hair-treatment preparations containing potassium bromate have caused acute renal failure and irreversible hearing loss.4,5 The time to peak serum bromate concentration after oral administration is 15 minutes in rat studies.5 Similarly, a 30-minute latency period for bromate in humans has been reported4; this correlates with the latency period observed in these outbreaks. Bromides were not identified in urine specimens from students involved in these outbreaks, although the results might have been affected by delayed collection of specimens or poor correlation between urine bromides and ingested bromate dose.4 Manufacturer A was alerted by FDA that calcium propionate and potassium bromate were present in the tortillas at higher than typical use levels and was advised to reduce the amounts used in the manufacture of these products. Manufacturer A changed the recipe and lowered the amount of calcium propionate and potassium bromate used in its product.

MDPH received notification of outbreaks in schools soon after the episodes occurred and was able to conduct complete epidemiologic investigations. Rapid identification and reporting of outbreaks enabled epidemiologists to collect the appropriate urine and food specimens for chemical analyses. These investigations highlight the need for collaboration with school officials, as well as interagency collaboration at local, state, and federal levels, for rapid response and collection of epidemiologic information, clinical specimens, and food samples. Local and state health officials are also encouraged to contact the Rapid Onset of Gastroenteritis with Unknown Etiology (ROGUE) workgroup at CDC (National Center for Infectious Diseases, Foodborne and Diarrheal Diseases Branch, and the National Center for Environmental Health, Division of Environmental Hazards and Health Effects) to obtain epidemiologic assistance and specialized laboratory analysis (telephone 770-488-3410 or 404-639-2206).

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