January 2001
volume 17 number 01
Division of Public Health http://health.state.ga.us
Kathleen E. Toomey, M.D., M.P.H. Director
State Health Officer
Epidemiology Branch http://health.state.ga.us/epi
Paul A. Blake, M.D., M.P.H. Director
State Epidemiologist
Mel Ralston Public Health Advisor
Georgia Epidemiology Report Editorial Board
Carol A. Hoban, M.S., M.P.H. - Editor Kathryn E. Arnold, M.D. Paul A. Blake, M.D., M.P.H.
Susan Lance-Parker, D.V.M., Ph.D. Kathleen E. Toomey, M.D., M.P.H.
Angela Alexander - Mailing List Jimmy Clanton, Jr. - Graphic Designer
Georgia Department of Human Resources
Division of Public Health Epidemiology Branch Two Peachtree St., N.W. Atlanta, GA 30303-3186 Phone: (404) 657-2588 Fax: (404) 657-2608
Please send comments to: Gaepinfo@dhr.state.ga.us
The Georgia Epidemiology Report is a publication of the Epidemiology Branch,
Division of Public Health, Georgia Department of Human Resources
Foodborne Outbreaks Associated with
Eating Pork Barbecue
Georgia 1996-2000
INTRODUCTION
Pork Barbecue (BBQ) is a major source of foodborne illness in Georgia. Since 1996, the Georgia Division of Public Health (GDPH) has investigated nine outbreaks associated with BBQ that were responsible for 815 cases of gastrointestinal illness and 52 hospitalizations. This report summarizes the major findings of five of the nine BBQ outbreak investigations. In all five investigations, food handlers did not properly monitor the internal temperature of the BBQ during cooking, cooling, and storage.
Outbreak 1-Bleckley County, August 1998 (1)
On August 18, the South Central District Health Officer notified the GDPH of an outbreak of salmonellosis. Three families and several local residents developed gastroenteritis after eating BBQ from a restaurant in Cochran, GA. Seven people were hospitalized. A case of gastroenteritis was defined as an illness that included at least two of the following symptoms: diarrhea, nausea, vomiting, fever, or chills. Fifty-one cases of gastroenteritis were identified with onset either in July (N = 18) or in August (N = 33). Forty-five of 51 case-patients recalled eating BBQ at the restaurant. Cultures of 14 stool specimens yielded Salmonella Typhimurium in 10 Salmonella isolates from five stool specimens and two BBQ samples were identical by pulsedfield gel electrophoresis (PFGE).
The restaurant owner reported that a meat packing plant near Cochran delivered pork twice a week. After delivery, the pork was immediately put into a pit of hot wood coals. After 11 hours of cooking, the pork cooled for 2-3 hours at room temperature. It was then transferred to a large 20-year-old refrigerator which had additional Freon added on August 7 because it felt unusually warm. The refrigerated pork was sold whole, sliced, or chipped. The pork was sliced and chipped at room temperature, a process that took up to one hour. Tables and utensils were used for both raw and cooked food preparation without appropriate cleaning.
Outbreak 2Habersham County, July 1999 (2)
On July 28, Habersham County notified the GDPH that several people became ill after eating at a local barbecue restaurant. Stool specimens from several ill residents yielded Salmonella sp. A case was defined as a person who had diarrhea and abdominal pain plus fever, chills or vomiting after eating at the restaurant. Twenty cases of salmonellosis with onset between July 16 and July 19 were identified. Besides diarrhea and abdominal pain, the most common symptoms were fever (85%), nausea (85%), chills (75%), vomiting (65%), and headache (60%). BBQ was the only food item statistically associated with illness (p=0.007). Three persons were hospitalized during their acute illness, including a woman pregnant with twins. She reported eating at the restaurant on July 16 and feeling ill with fever, diarrhea, and nausea that evening. On July 18, she went into premature labor and delivered twins via cesarean section at 35 weeks gestation. The infants were treated with intravenous antibiotics and released on July 21. Two days later the infants began to feed poorly and were readmitted. Both had Salmonella Typhimurium var Copenhagen isolated from their stools.
Stool specimens from eight case-patients yielded Salmonella. Seven of the eight isolates were available for serotyping and were identified as S. Typhimurium var Copenhagen. Culture of refrigerated BBQ leftovers from July 16 obtained from one patient detected S. Typhimurium var Copenhagen. The PFGE patterns of the S. Typhimurium isolates from patients, leftover BBQ, and the two infants were identical. Stool specimens from food handlers were all negative.
Fresh pork was purchased daily from a local grocery store and cooked in a pit the same day starting at 10:30 AM. After cooking, the pork stayed on the cooling pit to smoke. At 8:30 PM, the pork was placed in a refrigerator or pulled from the bone and then refrigerated. Peak cooking temperatures and refrigerated meat temperatures were acceptable, but a three-week
temperature log revealed that it took 2.5 to 4 hours for the pork to reach 140F. Also, the pulled pork was stored in 6-inch deep containers, too deep for rapid cooling. Food surfaces appeared clean and no obvious crosscontamination between cooked and uncooked food was observed.
Outbreak 3Hart County, September 1999 (3)
On September 14, Hart County notified the GDPH about a large number of illnesses after eating food from a local barbecue restaurant during the previous weekend. At first report, at least 20 people were ill and 7 were hospitalized. A case was defined as a person who ate at the restaurant on September 10-12 and who developed at least two of the following symptoms: diarrhea, fever, abdominal cramps, vomiting, or headache. Fifty-eight cases were identified. The mean incubation period was 19 hours. The most common symptoms were diarrhea (95%), cramps (88%), fever (87%), headache (67%) and vomiting (37%). Forty-one patients required medical attention for their illness and 25 of these were hospitalized. The only food statistically associated with illness was barbecue pork (p=0.0005).
Stool specimens from 20 ill persons yielded Salmonella Hadar, as did leftover samples of BBQ collected from the restaurant and from patients' homes. The PFGE patterns of isolates from patients' stools and from BBQ were identical.
Outbreak 4-Fannin County, September 2000 (4)
On September 18, Fannin County notified the GDPH that approximately 20 people had contacted their local emergency room regarding gastrointestinal symptoms following a local luncheon earlier in the day. Approximately 600 residents attended the luncheon that was catered by a local barbecue restaurant. A case was defined as a person who ate pork barbecue during the luncheon on September 16 and experienced at least one of the following gastrointestinal symptoms within 24 hours after eating: vomiting, nausea, diarrhea, or cramps. Eighty-seven (49%) of the 179 attendees contacted by phone were classified as cases. The mean incubation period was 2.75 hours. Persons 65 years old were 2.57 times more likely than younger attendees to be ill (p = 0.004). The most common symptoms were diarrhea (87%), nausea (82%), cramps (72%), and vomiting (77%). Thirty-one percent of the casepatients sought medical care for their symptoms. Those who reported an underlying medical condition were 24 times more likely to be ill (p < 0.0001). Those who ate food from the left buffet line were 25 times more likely than persons who ate on the right buffet line to report illness (p < 0.0001).
Two of 7 stool specimens from ill persons and 3 of 5 BBQ samples yielded enterotoxin-producing Staphylococcus aureus. All three BBQ samples contained enterotoxin as well. PFGE of the five isolates showed identical patterns. Nasopharyngeal specimens from two food handlers were negative for Staphylococcus aureus.
The environmental investigation conducted on September 18 found that the pork was delivered frozen to the restaurant twice a week. The pork was either cooked immediately or allowed to thaw in a refrigerator set at 41F. The pork was cooked in a large wood stove for approximately 24 hours and then pulled from the bone over several hours at room temperature. Once pulled, the pork was served immediately, placed in a warmer, or stored in a refrigerator. On the day of the luncheon the pulled pork was stored in a warmer in three 6-inch deep pans. On the day of the inspection, the pork in the warmer was at 143F while the fried chicken was at 133F. During the luncheon, the BBQ was served for two hours, warmed by a water table. Multiple luncheon attendees reported that the BBQ was cool when served.
Outbreak 5Catoosa County, September 2000 (5)
On September 24, the Tennessee Department of Health notified the GDPH of a large outbreak of gastroenteritis among approximately 900 people from throughout the Southeast who had attended a September 23 company picnic at a Georgia amusement park. An electronic questionnaire was distributed by e-mail to company employees to identify cases and to ascertain food histories. Preliminary analysis of the completed questionnaires suggested that the incubation period was 5-6 hours and that vomiting and diarrhea were the predominant symptoms. Approximately 380 employees became ill, with 2 hospitalized. Thirteen food samples and 11 human specimens were collected. Enterotoxin-producing Staphylococcus aureus was identified in several of the BBQ samples and in three of the eleven human samples. Environmentalists found that the temperature in the cooler where the food for the luncheon was stored rose from 50F to 60F during the night before the event.
DISCUSSION
Although these five BBQ-associated outbreaks occurred throughout Georgia and involved different food handlers, the factors that may have contributed to the outbreaks were similar. Reports from three of the outbreaks stated that the time allotted to cook the BBQ extended from 12-24 hours. Despite this long cooking period, thermometers were not used to document the temperature of the cooking pork. BBQ is cooked at relatively low temperatures; higher temperatures for such a long time would render the BBQ dry and unappetizing. In some instances the pit was allowed to cool after cooking so that the BBQ could smoke for several hours, again without monitoring the internal temperature of the meat.
After the pork was cooked and in some instances smoked, it was sliced, "pulled" (the meat is pulled from the bone), or stored in a refrigerator. In three of the outbreaks, the slicing or pulling occurred at room temperature and took several hours, a period of time that was relatively long because the restaurant was preparing for a large event. Prolonged handling of BBQ can increase the likelihood of contamination by bacteria and of subsequent multiplication. Once sliced or pulled, the pork was transferred to either a refrigerator or a warmer. In several of the outbreaks, the refrigerators were set at the appropriate temperatures, but the temperature of the refrigerated meat was never checked with a thermometer. The use of pans 4 inches deep to store the meat in two outbreaks inevitably prolonged heating and cooling, allowing the meat to remain at unsafe temperatures for extended periods (6). Contaminated meat stored above 41F or below 140F allows bacteria to multiply, and in the case of S. aureus, to produce toxin. Reheating BBQ after S. aureus toxin has formed will not destroy the heat stable toxin.
Although infected food handlers or contaminated equipment could have contributed to these outbreaks, improper temperatures, exhibited either by failing to reach appropriate cooking temperatures or allowing food to remain at unsafe temperatures for extended periods, certainly played a role. Failing to use a thermometer to measure the temperature of the pork throughout the cooking and serving process was the most commonly noted food handling error in these investigations.
Food handlers and consumers should be aware that preparation of barbecue pork is inherently risky, particularly when large batches are made, due to the extended time spent cooking, smoking, and handling the pork. Proper holding temperatures following cooking are necessary to prevent foodborne outbreaks and can be monitored easily with an inexpensive thermometer (7). One of the problems frequently encountered in BBQ preparation is that the cooks have often used the same methods for many years without causing any recognized outbreaks, have been lulled into complacency, and find it difficult to believe that any changes in their practices are necessary.
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FOOD SAFETY GUIDELINES
STORAGE Cook or freeze pork within 3-5 days after purchase. Set freezer at 0F. Place thermometers inside freezers and refrigerators and monitor regularly.
DEFROSTING Thaw in a refrigerator set at 41F, not at room temperature. Completely thaw pork before cooking to promote even cooking.
COOKING Use a thermometer to ensure that the pork reaches a safe internal temperature and monitor regularly. Pork should reach 155F for >15 seconds. After cooking, keep the meat at >140F or cool it rapidly to prevent bacterial growth and toxin production.
DEBONING Keep deboning time as short as possible. After deboning, immediately reheat the pork to >155F for >15 seconds to kill any contaminants. After reheating, maintain the meat at >140F.
SERVING Keep pork at room temperature for <2 hours. When room temperature is >90F (e.g., a hot kitchen or a hot summer day), keep pork at room temperature for <1 hour.
HANDLING LEFTOVERS Discard pork held at room temperature >2 hours. Discard pork left out at >90F for >1 hour. Store leftovers in pans <4 inches deep and <2 hours after taking pork off grill to promote efficient cooking and cooling at center of pan.
FOOD HANDLERS Meat handlers must be healthy and have no open sores. Food handlers should wash their hands immediately after eating, drinking, using the toilet, handling potentially contaminated food, or using tobacco
products.
Most of these recommendations can be found in the Georgia Rules and Regulations for Food Service (9).
REFERENCES
1. Samuelson J and Fiore A. Outbreak of Gastroenteritis caused by Salmonella typhimurium Associated with a Restaurant in Cochran, GA. Report of Investigation: GDPH; September 25, 1998.
2. Williams K, Axelson, L, Bennett T, and Benson J. Outbreak of Salmonella typhimurium Infections Associated with a Barbecue Restaurant. Report of Investigation: GDPH; October 1, 1999.
3. Rebmann C and Tomashek K. September 1999 Outbreak of Salmonella ser Hadar with a Barbecue restaurant in Hart County, GA. Report of Investigation: GDPH; January 19, 2000.
4. Kramer S and Wootton, S. Outbreak of Staphylococcus aureus Intoxication Associated with a Barbecue Pork Lunch in Fannin County, GA. Report of Investigation: GDPH; November 15, 2000.
5 Thomas S and Fletcher J. Foodborne Outbreak in Catoosa County. Report of Investigation: GDPH; September 23, 2000.
6. http://www.fsis.usda.gov/OA/pubs/cibarbecue.htm
7. Centers for Disease Control. Foodborne Disease Outbreaks: 5-yr Summary, 1983-1987. Morbidity and Mortality Weekly Report. 1990; 39(SS-1):39-59.
8. Chin J. Control of Communicable Diseases Manual, 17th ed. Washington, DC: American Public Health Assoc.; 2000
9. http://www.ganet.org
This article was written by Susan H. Wootton, M.D.
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The Georgia Epidemiology Report Epidemiology Branch Two Peachtree St., NW Atlanta, GA 30303-3186
PRESORTED STANDARD U.S. POSTAGE
PAID ATLANTA, GA PERMIT NO. 4528
January 2001
Volume 17 Number 01
Reported Cases of Selected Notifiable Diseases in Georgia Profile* for August 2000
Selected Notifiable Diseases
Total Reported for October 2000
2000
Previous 3 Months Total
Ending in October
1998
1999 2000
Previous 12 Months Total
Ending in October
1998
1999
2000
Campylobacteriosis
40
Chlamydia trachomatis
2649
Cryptosporidiosis
18
E. coli O157:H7
2
Giardiasis
71
Gonorrhea
1912
Haemophilus influenzae (invasive)
6
Hepatitis A (acute)
24
Hepatitis B (acute)
11
Legionellosis
2
Lyme Disease
0
Meningococcal Disease (invasive)
2
Mumps
0
Pertussis
0
Rubella
0
Salmonellosis
167
Shigellosis
28
Syphilis - Primary
6
Syphilis - Secondary
27
Syphilis - Early Latent
34
Syphilis - Other**
67
Syphilis - Congenital
0
Tuberculosis
44
223
181
135
6538
8868
8716
61
48
61
29
14
9
440
467
322
5459
6615
5831
14
8
11
279
123
117
36
74
73
2
4
3
0
0
0
19
13
6
0
3
0
9
14
5
0
0
0
806
756
607
254
79
86
28
37
27
57
86
87
181
157
130
223
208
212
2
9
3
150
151
177
808 20158
140 79 1204 17039 59 868 224 11 6 102 2 35 0 1766 1345 124 242 869 886 12 616
752 32198
173 41 1309 22285 81 574 220 4 0 75 5 48 0 1991 370 140 281 733 766 23 632
605 29999
188 50 1244 19642 80 330 261 10 0 55 2 49 0 1738 290 125 309 603 725 14 678
* The cumulative numbers in the above table reflect the date the disease was first diagnosed rather than the date the report was received at the state office, and therefore are subject to change over time due to late reporting. The 3 month delay in the disease profile for a given month is designed to minimize any changes that may occur. This method of summarizing data is expected to provide a better overall measure of disease trends and patterns in Georgia.
** Other syphilis includes latent (unknown duration), late latent, late with symptomatic manifestations, and neurosyphilis.
Report Period
Latest 12 Months: 11/99 - 10/00 Five Years Ago: 11/94 - 10/95 Cumulative: 7/81 - 10/00
Total Cases Reported*
Percent Female
AIDS Profile Update
Risk Group Distribution (%) MSM IDU MSM&IDU HS Blood
Unknown
1242
26.7
28.1
10.5
2.4
12.7
2
44.2
2327
19.1
47.1
20.6
5.7
15.6
1.7
9.2
22454
16.6
48.9
18.5
5.7
13
1.9
12
MSM - Men having sex with men
IDU - Injection drug users
HS - Heterosexual
* Case totals are accumulated by date of report to the Epidemiology Section
- 4 -
Race Distribution (%) White Black Other
18.8 77.9
3.3
35.3 62.3
2.4
36.1 61.8
2.1