Outbreak of Salmonella Enteritidis, Athens County, May, 2010

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1 Outbreak of Salmonella Enteritidis, Athens County, May, 2010 Title: Athens Salmonella_May 2010 Jurisdiction: Athens County Type of outbreak: Foodborne OB ID: ODRS ID: CDC NORS ID: BACKGROUND: Athens City County Health Department (ACCHD) received initial notification on May 5, 2010 of 4 patients admitted to the local hospital in the preceding 24 hours with nausea, vomiting, and diarrhea. One person had a positive lab result for salmonella. All case patients reported eating at the same local Mexican food restaurant. In addition to the 4 hospitalized patients, the spouse of one of the case patients who shared the meal at the local restaurant was also reported ill. After interviews with case patients, it was hypothesized that the case patients had contracted salmonella after eating at a local Mexican food restaurant in Athens, Ohio, (Restaurant A). The restaurant investigated in relation to this outbreak is a local Mexican food restaurant that serves lunch and dinner. The restaurant seats 100 people and offers a carry out menu. The menu items are prepared from scratch in house. The kitchen has two hand wash sinks available to cooks and staff in the approximately 400 square foot kitchen in addition to an employee restroom. Methods used included environmental inspections, interviews, laboratory results, and a case control study. Chiles rellenos were statistically associated with illness (Odds Ratio = 21.38) particularly those with the earliest exposures and illness onset dates. Recommendations to avoid this problem in the future include following guidelines to reduce the risk of Salmonella Enteritidis and the Food and Drug Administration Food Code and applicable state and local regulations including the Ohio Uniform Food Safety Code. Salmonellosis is an infection caused by rod- shaped, Gram- negative bacteria called Salmonella. Most persons infected with Salmonella develop diarrhea, fever, and abdominal cramps 12 to 72 hours after infection. The illness usually lasts 4 to 7 days, although the course of illness may be longer. Most persons recover without treatment; However, the diarrhea may be so severe that hospitalization is necessary. In some patients, the Salmonella infection may be more severe, spreading from the intestines to the blood stream, and other body sites. The elderly, infants, and those with impaired immune systems are more likely to have a severe illness. There are over 1500 serotypes of Salmonella. Salmonella serotype Enteritidis is the most common in the United States.

2 Salmonella serotype Enteritidis is frequently associated with consuming raw or undercooked eggs or egg products. Salmonella enteritidis bacterium can also be transmitted through foods or drinks that have become contaminated with the bacterium. METHODS: Following the initial report, demographic information was obtained on the hospitalized case patients, and the spouse of one of the hospitalized case patient. Additional reports of illness came to the ACCHD as a result of routine surveillance and reporting, and self- reporting due to media reports and word of mouth. The following activities occurred as part of the investigation: The Ohio Department of Health (ODH) was notified and information regarding the outbreak was entered into the Ohio Disease Reporting System and the National Outbreak Reporting System; Interviews were conducted with case patients to gather food history and other exposure information Stool specimens were submitted for testing to the ODH Laboratory and many were subjected to further testing by the Centers for Disease Control and Prevention (CDC). Leftover meal samples, menu item, and product samples were submitted for laboratory testing An Ohio Public Health Communications System (OPHCS) Alert was issued to notify public health partners and call for cases of salmonellosis with a history of visiting Athens or eating food from Athens in the past week Case control study Environmental inspections; and Laboratory testing of food handlers from restaurant being investigated. METHODS: EPIDEMIOLOGIC Case Classification Confirmed: A case that is laboratory confirmed and who consumed food from Restaurant A. Probable: A clinically compatible case that is epidemiologically linked to a confirmed case and who consumed food from Restaurant A. Suspect: A clinically compatible case that is not yet laboratory confirmed and is not epidemiologically linked to a confirmed case. Clinical Case Definition: An illness of variable severity commonly manifested by diarrhea, abdominal pain, nausea, and sometimes vomiting.

3 Secondary Case: A confirmed, probable, or suspect case of salmonella who was a household contact of a confirmed case who did not consume food from Restaurant A. Members of the ACCHD environmental and nursing staff conducted interviews of case patients to determine 72 hour food history and other potential salmonella exposures. In addition, a case control study was conducted utilizing a questionnaire with specific exposure questions about food items consumed at the restaurant under investigation. Answers to the questions from the questionnaire were entered into SurveyMonkey which was utilized to compile results. MICROBIOGICAL Stool specimens: Modified Cary Blair Medium was used for the transport of stool specimens which were collected by the individual case patient or food handler. Additional specimens were submitted directly from health care providers to the ODH Laboratory. Serotyping, MLVA, allele typing, PFGE, results were obtained for 38 specimens with phage typing results obtained for four of the 38 specimens. MLVA, allele typing, PFGE, and phage typing were conducted by the Centers for Disease Control and Prevention (CDC). Food specimens: Food samples of chiles rellenos were collected on site at the restaurant. The chiles rellenos were collected from a sheet pan sitting on the counter and had been reheated. They were reportedly from the batch prepared the weekend preceding May 5, At the time of collection they were at 96 degrees Fahrenheit. The chiles rellenos were packaged, kept refrigerated and transported on icepacks to the ODH Laboratory. 1 thawed and opened container (1/2 gallon carton) of liquid egg whites (pasteurized) was collected, was kept refrigerated, and was transported on icepacks to the ODH Laboratory. At the time of collection they were at 43 degrees Fahrenheit. Samples were collected from three separate trays of frozen chiles rellenos and transported in a frozen state to the ODH Laboratory. A left over meal was brought to the ACCHD by a case patient, was kept refrigerated, and transported on icepacks to the ODH Laboratory. The leftover meal was in a Styrofoam clamshell container and included leftover chiles rellenos, chips, salsa, spinach burrito, enchiladas, and guacamole. Additional testing from this specimen was conducted by CDC to provide MLVA, allele type, PFGE pattern and phage typing. Product specimens: 8 cartons (1/2 gallon size) of liquid egg whites were received frozen and transported in a frozen state to the Ohio Department of Agriculture, Consumer Analytical Laboratory. These were labeled A- H. ENVIRONMENTAL The initial outbreak inspection occurred in the afternoon of May 5, 2010 after a reportedly busy lunch at the restaurant due to Cinco de Mayo celebration. The conditions during the busy lunch rush were speculated to be similar to the conditions at the restaurant during the reported exposure times the

4 weekend before which was Ohio University Mom s Weekend, contributing to an increase in the number of diners at local restaurants. A total of four sanitarians participated in the inspection. Three sanitarians inspected the kitchen while one sanitarian explained the foodborne illness concerns to the assistant manager, who was the person in charge at the time of the inspection. Each subsequent inspection and sampling was conducted with at least two sanitarians present. The restaurant cooperated fully with the inspections and the investigation. The menu item initially implicated was removed voluntarily by the restaurant when notified of the problem. Results of the inspections were documented utilizing the Ohio Department of Agriculture/Ohio Department of Health Standard Inspection Report form. Four inspections were conducted following the initial inspection. RESULTS: EPIDEMIOLOGIC A total of 77 interviews were conducted with 71 via telephone and 6 in person. From interviews information was provided by the case patient regarding symptoms they experienced, food history and other possible exposures. Interviews of 21 well meal companions provided additional food exposure information. Environmental health staff conducted interviews at the hospital and learned that all of the initial case patients, had eaten at the same local Mexican food restaurant over the weekend, and all of the case patients, except one, had consumed chiles rellenos while dining at the restaurant. The one who had not eaten the chiles rellenos had dined with another case patient who had eaten the chiles rellenos. Public health nurses interviewed the additional case patients as they were identified. Of the 56 case patients entered into the Ohio Disease Reporting System (ODRS), 47 reside in Athens County, including some with temporary Athens County Residence *83.93%, N=47), 1 resides in Fairfield County, 1 in Franklin County, 3 in Meigs County, 1 in Morgan County, 1 in Stark County and 2 in Tuscarawas County. 33 of the case patients are females and 23 are male. Ages of case patients ranged from 5 years of age to 82 years of age, with a median age of 33.5 and mean age of At least 7 (12.5%, N= 7) of the case patients were known to have been hospitalized due to the illness. Of those hospitalized, 4 were female and 3 were male. Of the case patients hospitalized, their ages ranged from 19 to 82, with a median age of 48 and a mean age of Common symptoms of salmonellosis enteritidis included nausea, cramps, diarrhea, fever, chills, headache, and body aches. Illness onset dates of confirmed cases ranged from May 1, 2010 through May 14, Of the confirmed cases, 38 reported an illness onset date. The usual incubation period for salmonella enteritidis is hours making most common exposures likely range from April 28 through May 8, 2010.

5 Figure 1: Chart displaying the illness onset dates reported by case patients with confirmed, probable, and suspected cases of salmonellosis enteritidis who reported an illness onset date # OF SUSPECTED CASES # OF PROBABLE CASES # OF CONFIRMED CASES 5/2/2014 5/3/2014 5/4/2014 5/5/2014 5/6/2014 5/7/2014 5/8/2014 5/9/2014 5/10/2014 5/11/2014 5/12/2014 5/13/2014 5/14/2014 5/15/2014 Table1: Summary of reported cases Case Classification Status Number of Cases Percentage of Cases Confirmed % Probable % Suspected % Total % Interviews with the 18 initial case patients led to the early hypothesis that the chiles rellenos were involved in the transmission of the illness. The 18 initial case patients had dined at the restaurant between April 29, 2010 and May 1, 2010 with illness onset dates ranging from April 30, 2010 to May 4, Of the 18 initial case patients, 17 of them had eaten the chiles rellenos. The only one who had not eaten the chiles rellenos had dined with her husband who had eaten the chiles rellenos and was also ill. The majority of these cases reported eating with others who were not ill and who had eaten menu items other than the chiles rellenos. The chiles rellenos are prepared in the following manner according to the person in charge at the restaurant: Poblano peppers are received once a week and are washed and cored

6 The cored poblano peppers are then stuffed with white cheese which is shredded on- site The stuffed peppers (chiles rellenos) are then dipped in the pasteurized egg white product and floured Next, the chiles rellenos are deep- fried Once deep- fried, the chiles rellenos are ready to eat and can be plated to be served immediately or frozen to be reheated in the oven before serving. A case control study, in which 79 interviews were conducted, resulted in a strong association of eating chiles rellenos with becoming ill with Salmonellosis enteritidis. Two interviews were dropped from analysis because their restaurant dates were after 5/5/10. A total of 77 interviews, 47 cases and 30 controls (well meal companions), were included in the study. Six (cases- 4 and controls- 2) were dropped because consumption of chili rellenos were unknown. No other food emerged as a suspect food. Table2: Case control study summary of chiles rellenos exposure: Sum of Counter Type of Interview Chiles Rellenos Case-Patient Dining Companion Grand Total Yes No Grand Total Odds Ratio = (2.65 <OR<460.00) Uncorrected Chi- Square: P- value: MICROBIOLOGICAL Stool specimens: Salmonella Enteritidis, was determined from laboratory testing to be the serotype of salmonella that caused this outbreak. Of the 56 cases of salmonellosis associated with this outbreak through the Ohio Disease Reporting System, 41 of them were found to be infected with Salmonella enteritidis through serotyping. Of the 42 confirmed cases, 41 of them were positive for Salmonella enteritidis and one, though positive for salmonella was of an undetermined serotype. Further testing of the stool specimens was conducted by the Centers for Disease Control and Prevention, due to a shared food ingredient with another foodborne outbreak in North Carolina. Multiple- Locus Variable number tandem repeat Analysis (MLVA), allele typing, and Pulse Field Gel Electrophoresis (PFGE)pattern testing was conducted. Phage testing was also conducted on 4 of the specimens. A total of 48 stool specimens were submitted to CDC under the suspicion that they may be part of this outbreak. 8 of the specimens, though identical matches by MLVA, allele typing, and PFGE, were not included as cases in the outbreak due to poor or no food history or a food history that did not include exposure to the restaurant being investigated. 38 of

7 the records matched exactly by MLVA, allele typing, and PFGE. The remaining two specimens were not matches to each other or the other cases. A spreadsheet of the results is included in the supporting documents. Results of the 38 specimens from case patients considered to be part of this outbreak are: MLVA: A Allele Type: PFGE: Phage testing was also conducted on 4 of the specimens and all resulted in phage type 13. The 9 stool specimens submitted by the food handlers directly involved in the preparation of the food during the exposure times of the case patients were negative for salmonella. Food specimens: The chiles rellenos collected on May 5, 2010 tested negative for Salmonella. The thawed and opened container (1/2 gallon carton) of liquid egg whites (pasteurized) tested negative for salmonella. Samples from the three frozen trays of chiles rellenos all tested negative for salmonella. The one leftover meal yielded the following test results, an identical match to the 38 specimens that were part of the outbreak, the case patient who submitted the leftover meal, and the four specimens that were phage typed: MLVA: A Allele Type: PFGE: Phage Type: 13 Product specimens: No salmonella were detected in specimens A- H which consisted of 8 cartons of pasteurized liquid egg whites in unopened ½ gallon cartons. ENVIRONMENTAL The Athens City- County Health Department (ACCHD) conducted the initial inspection of the entire facility on May 5, Four sanitarians conducted this inspection. Interviews with case patients initially implicated the chiles rellenos. The assistant manager explained their process of preparing the chiles rellenos and voluntarily removed this item from the menu. Critical violations were noted during this inspection and samples of the implicated menu item were taken.

8 Critical violations follow. HOT HOLDING HAZARD: Hot holding shall be 135 degrees Fahrenheit or above. Discard any time/temperature controlled for safety food products which have been between degrees Fahrenheit for four hours or more. o Observed chiles rellenos holding at, 96.7 degrees Fahrenheit. COLD HOLDING HAZARD: Cold holding shall be 41 degrees Fahrenheit or below. o Observed food products in the walk- in cooler cold holding at between degrees Fahrenheit including chiles rellenos at 46.0 degrees Fahrenheit. o Observed food products cold holding at degrees Fahrenheit in the preparation table. o Observed food products cold holding at 43 degrees Fahrenheit in the small cold holding table.. o Observed food products cold holding at 45 degrees in the double door reach in cooler. CROSS CONTAMINATION HAZARD: If used, single- use gloves shall be used for only one task such as working with ready- to- eat food or with raw animal food, used for no other purpose, and discarded when damaged or soiled, or when interruptions occur in the operation. o Observed food preparation employee wash hands, put on gloves, handle raw steak, and then, with the same gloves, handle ready to eat vegetables, tortillas, and utensils, posing a cross- contamination hazard. Raw animal products shall be stored below or separate from ready to eat food products. o Observed raw animal products being stored above ready to eat food products in the walk- in freezer. All food products shall be covered while in storage in order to prevent contamination. o Observed food products uncovered in storage, including chiles rellenos in walk- in freezer. Hand washing supplies must be available at all times at all hand wash sinks. o Soap was not available at the hand wash only sink located near the bathroom. DATE MARKING HAZARD: All potentially hazardous food products open from the original container and kept over 24 hours must be date marked with the seven day expiration date. o Did not observe date marking on any food products in storage. Critical violations were either corrected, food items discarded, or maintenance was scheduled.

9 The ACCHD conducted follow- up Inspections on May 6, 7, 12, and 17 by at least two sanitarians. During these inspections, more samples of menu items and ingredients were taken for testing and all violations noted were either corrected or food items were discarded. Critical violations observed on May 6, 2010 follow. COLD HOLDING HAZARD: Cold holding shall be 41 degrees Fahrenheit or below. o Observed the large prep table holding potentially hazardous food products at degrees Fahrenheit. o Potentially hazardous foods were holding at 46-47degrees Fahrenheit in the walk in cooler. Critical violations observed on May 7, 2010 follow. HOT HOLDING HAZARD: Hot holding shall be 135 degrees Fahrenheit or above. Discard any time/temperature controlled for safety food products which have been between degrees Fahrenheit for four hours or more. o The rice mixture was not placed on the steam table and was holding at 127 degrees Fahrenheit. COLD HOLDING HAZARD: Cold holding shall be 41 degrees Fahrenheit or below. o Cold holding temperatures in the walk in cooler are 48 to 62.3 degrees Fahrenheit in the walk in cooler. o Double door reach in refrigerator cold holding temperature is also elevated to 42.5 degrees Fahrenheit. o Double refrigerator temperature was not holding cold enough with temperature of milk at 43 degrees Fahrenheit. CROSS CONTAMINATION HAZARD: Hand washing supplies must be available at all times at all hand wash sinks. o No towels were found in the employees restroom sink. On May 12, 2010, critical violations were as follows. COLD HOLDING HAZARD: Cold holding shall be 41 degrees Fahrenheit or below. o Double refrigerator temperature was not holding cold enough with temperature of milk at 43 degrees Fahrenheit.

10 Additionally, on May 12, 2010, ACCHD received 8 cartons (1/2 gallon size) of liquid egg whites. 1 Carton was thawed and opened. The other 7 were frozen and unopened. No liquid egg whites used in the production of the chiles rellenos that were served during the time that the initial case patients consumed the suspect meal remain as all had been used in the production. On May 17, 2010, no violations were observed. Samples were collected from three separate trays of frozen chiles rellenos which had been prepared in a similar manner to the implicated food item. The restaurant was fully cooperative during this investigation. Copies of all inspections are located in the Supporting Documents section. DISCUSSION: Early in the investigation, a single menu item, chiles rellenos, drew attention as a source of the salmonella infections. This was based on the early case/control interviews and positive Salmonella test results from a leftover meal sample. The ingredients of the chiles rellenos (along with the prep procedure and storage of the item) were carefully considered as possible sources of the bacterial contamination. A product in common with the Salmonella enteritidis outbreak in North Carolina, packaged pasteurized egg whites, was especially suspect due to the nature of the material (egg white) and the coincidence of the NC outbreak. Lab test results of prepared chiles rellenos, samples of the unused pasteurized egg product from the local restaurant, the NC restaurant and the manufacturing facility did not support a hypothesis that the Salmonella originated from the pasteurized product. Opportunities for cross contamination also were observed including improper use of single- use gloves, and the storage of raw animal products above uncovered chiles rellenos. Hot holding and cold holding conditions observed at the restaurant were conducive for the growth of bacteria. Microbiological testing supports the hypothesis of the common food source as well. Actions taken to protect the public health included: Voluntary removal of the suspect menu item during investigation of the outbreak to reduce the risk of others consuming a possibly infectious ingredient; Provision of information to the public regarding general food safety measures to reduce the risk of acquiring salmonellosis and other food borne illnesses; Provision of education to the person in charge regarding the violations and measures necessary to correct them; and Repeat inspections to ensure that the violations were corrected and appropriate standards are being met to continue the food service operation.

11 RECOMMENDATIONS: Corrective action taken by the Athens City County Health Department was to make hand washing supplies available at all hand wash only sinks at all times, cover food products in storage to prevent contamination, observe date marking system, store raw animal products below or separate from ready to eat products, observe appropriate hot and cold holding, and properly use single- use gloves. Initially, on May 5, food safety booklets in Spanish were distributed to the staff of Casa Lopez and these were immediately read by each staff member. Regular inspections will continue at this food service establishment. Also a Level One Food Safety Training course will be given to the staff. These corrective measures have already been implemented. SUPPORTING DOCUMENTS: Athens County Health Department Answering Service Log Questionnaire utilized for case control study Clinical specimen and left over meal lab results spreadsheet Ohio Department of Agriculture/Ohio Department of Health Standard Inspection Reports (Dated 05/05/2010, 05/06/2010, 05/07/2010, 05/12/2010, and 05/17/2010) REFERENCES: Salmonellosis. Web. 3 Sep < Salmonella Enteritidis. Web. 3 Sep <

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