Hazard Analyses of Char siu and Roast Pork in Chinese Restaurants and Markets

422 Journal of Food Protection, Vol. 45, No.5, Pages 422-429 (Aprill982) Copyright International Association of Milk, Food, and nvironmental Sanitarians Hazard Analyses of Char siu and Roast Pork in Chinese Restaurants and Markets FRANKL. BRYAN I*, CHARLS A. BARTLSON2, MITSUTO SUGI3, BATRIC SAKAI3, LLOYD MIYASHIR3, STVN TSUTSUMI3 a.nd CLIFFORD CHUN3 U.S. Department a;f'health and Human Services, Public Health Service, Centers for Disease Control, Washington State Department of Social and Health Services. and Hawaii State Department a;f'health (Received for publication March 25, 1981 l ABSTRACT valuations of time-temperature exposure of each stage of the preparation of char siu (marinated roast pork) were made at six Chinese restaurants and a market. These evaluations were also made of roast pork at the market. Samples of these products at the various stages of preparation and swabs of equipment surfaces that the pork touched during preparation were tested for Clostridium perfringens, Salmonella and Staphylococcus aureus. The water activity of other samples was also determined. Temperatures attained at the geometric center of these pork products during roasting in ovens or after cooking ceased were such that vegetative pathogenic food borne bacteria should have been killed, if present. The cooked products were often displayed in warming cabinets or window counters at which time their temperatures were within a range that would permit rapid bacterial growth for several hours. Reheating of leftover pork was inadequate to destroy pathogenic microorganisms that grew or toxins that were produced during storage. The water activity of char siu was frequently at a level that would increase the bacterial lag phase and slow the rate of growth of pathogenic bacteria from optimum. A few samples of char siu were contaminated by low numbers of C. perfringens and a sample of raw and roast pork with S. aureus. There were opportunities for contamination of cooked pork products during preparation, particularly at the market. Critical control points for these operations--handling after cooking, hot-holding, cooling and reheating--are given along with measures for controlling and monitoring these points. Foods prepared in Chinese restaurants have been reported as vehicles of foodborne disease outbreaks (6,7.1,12,13). Boiled rice and fried rice have often been incriminated as vehicles, but, in many other investigations, specific vehicles have not been identified. Cured 1 U.S. Department a;l Health and Human Services. Public Health Service, Centers for Disease Control. Atlanta. Georgia 3333. 2 Washington State Department a;( Social and Health SeT'I!ices, O{vmpia, Washington 9854. 'Hawaii State Department ofhealth. Honolulu. Hawaii 9681. pork (ham) and barbecued pork that have been prepared in foodservice establishments other than Chinese restaurants have often been identified as vehicles of foodborne illness <;!,5,12,13). Char siu, which ts marinated roast pork but is often referred to as barbecued pork, prepared in Chinese restaurants has only rarely been incriminated (1,15). Yet, because this product is quite popular and consequently is kept available for serving, it often remains for long periods of time within a temperature range that is suitable for growth of food borne pathogenic bacteria. Whether this apparent failure to be a vehicle in foodborne disease outbreaks could be real or a result of the lack of reports or incomplete investigations has not been examined. The purpose of this investigation was to (a) ascertain hazardous operations associated with the preparation and storage of pork products in several Chinese restaurants and in a Chinese market, (b) to relate these findings to the water activity of the product, and (c) to identify critical control points of typical preparation activities. MATRIALS AND MTHODS Operations Char siu is pork loin cut into rectangular strips approximately 3 em (1.2 in) by 6 em (2.4 in) and 2 to SO em (8 to 2 in) long that is marinated in a solution of sugar. salt, spices, soy sauce and red dye. It is usually refrigerated overnight and is then roasted in a gas-fired oven. After cooking. the char siu is either left in the unheated oven, stored in pans in a walk-in refrigerator. held at room temperature in pans, or stored in a display cabinet or on counters by a window. This product is either sold whole for take out orders or thinly diced into small pieces (<1 em thick) for use in won ton soup. fried rice or other dishes. Sides of fresh hog carcasses were left overnight at room temperature. Salt was rubbed over the surface and into cuts made in the flesh. After roasting in an oven. the sides were cut into chunks of roast pork and stored in glass cabinets until sold. Operations involved in preparing char siu were evaluated in six restaurants (A. B. C. D.. F) and at a market (G) that were located in either the states of Hawaii or Washington. Operations for preparing the cuts of roast pork were evaluated at the market. i\1 easureme,1ts Water activity (aw) was evaluated with an electric hygrometer. JOURNAL OF FOOD PROTCTION. VOL. 45, APRIL 1982

HAZARD ANALYSS OF CHAR SIU 423 Specifications for this instrument have been published (6). Recordings were usually made at 25 C (77 F), however, a few recordings were made at other temperatures. Several samples were frozen and thawed before analysis for- Time-temperature measurements were obtained with thermocouples and recorded on a recording potentiometer. Specifications for this instrument have been published -6). Necdle point thermocouples were inserted into the meat so that the sensing end was located near the geometric center. Welded-junction thermocouples were used to measure air temperatures. Laboratory Samples for laboratory analysis were taken as described by Bryan et al. (4.6). Laboratory procedures for the isolation of Clostridium perfringens, Salmonella and Staphylococcus aureus are described in the Bacteriological Analytical Manual (} 6). RSULTS AND DISCUSSION Storage of raw products Temperature changes in a side of raw pork (at the center of a thigh) held overnight at room temperature are shown in Fig. 1. The temperatures were such that psychrotrophic and mesophilic microorganisms could have multiplied for several hours. Temperatures of strips of raw pork, during marinating in a refrigerator, are shown in Fig. 2. During this period, usual pathogenic foodbome bacteria would not be expected to multiply because of the combined effects of low temperature and salt concentration. cooking are summarized in Table 1 and examples are illustrated in Fig. 3-7. The highest temperatures attained at the geometric centers of pieces of char siu ranged from 61 C (142 F) to 91 C (195 F). Internal temperatures of the roast pork reached 74 C (166 F) and 81 C (178 F). The temperatures rose as much as 4 C (7 F) after cooking ceased. According to established D-values for various pathogenic bacteria in similar substrates (1,8), the time-temperature values attained in these products should have killed most vegetative pathogenic foodborne bacteria that might have been present. Oven a;r Out of oven and to refrigerator * ---165 F -- 15 F. Figure 3. Temperatures at geometric center of char siu during cooking in an oven and during cooling in a walk-in refrigerator (F;stablishment A). >-fot:rs Figure 1. Temperatures at center of thigh of side of uncooked pig carcass during hanging at room temperature (F;stablishment G). Figure 4. Temperatures at geometric center of char siu during cooking and during cooling at room temperature and in a walk in refrigerator I,F;stablishment C). Figure 2. Temperatures of.6-lb strip of char siu marinating in a walk in refrigerator (F;stablishment F). Cooking Time-temperature exposures of char siu during Handling cooked products Cooked pork products were often handled by workers who had previously handled raw meat or raw poultry. The cooked products were chopped and sliced on cutting boards with cleavers and knives that were also used for other purposes. The cooked pork could easily have become contaminated during this operations because S. JOURNAL OF FOOD PROTCTION, VOL. 45, APRIL 1982

424 BRYANTAL. IT 325 / :Oven air 175. 15 J. ll 25. 125. Q) 225..2 2. 11. I Q; 175 ----15 F----------------------65socl l 75 Char siu 5 1 15j'_ r-- 125 75 25 Room air 5 25,,-,,-,-,-,,-,-,-,,-"-, 2 3 4 56 7 8 911 1 11213141516171819 Figure 5. Temperatures at geometric center of char siu during cooking and during subsequent holding at room temperature (stablishment ). 1:11) :::: :::: - 4-.p ::;;..::: -------- oolfllfloooo-vln -,olfloo-.d-.d-.d\"<1" t-- -.D 5 475 45 Oven a1r 425 4 375 35 ll 325 3 I 2 275 :; 25 Q. 225 '"' 2 175 15 125 1 75 t Meat removed 5 from oven and 25 holes poked through sk1n 25 225 r75 S1de 1 t15 out of oven Q) Pork s 1de 1, S1de 1... d 125.2 2 Char stu ( center of cutdup. eat ;emoved th1gh meat noved oven 1 rom ven to the._ i OJ market ; I- ' [-75 15o F--.- -,=:/,(;$;- = -, 65 soc! SO -==.:::::--. Porks1deZ,centerr ----'---- -- =- - - of shoulder meat 1 Center of t ' 25 Char stu Side 2 1nto oven Figure 6. Temperatures of pork sides and marinated strips of char siu during cooking and room-temperature storage (stablishment G). aureus and C. perfringens were frequently isolated from swab samples of utensils, equipment or cloths in the market, but they were not isolated from swab samples taken in restaurant F (Table 2). Display After cooking, char siu and other pork products were sometimes displayed in "warming" cabinets or window counters. Glass on three sides of the cabinets protected the pork from contamination by customers and certain other sources. A few infrared and incandescent light bulbs, within the cabinet or window display area but usually at a considerable distance from the food, were used to heat the air around the pork. Time-temperature exposures under such circumstances are shown in Fig. 7, 8 and 9, and summary data are given in Table 3. Whenever the pieces of pork were not sold soon after they 4 JOURNAL OF FOOD PROTCTION. VOL. 45. APRIL 1982

4758 45.. 425 :. 4 Oven air 375 HAZARD ANALYSS OF CHAR SIU 425 225 2 35. 175 )25. 3. 15 e 275 u ::::l 25 125 Q),._ "'- ::::l :g_ 225-1,._ Q) 2 Q) a. r:- 175 75 15 125 5 1 75 Display area air 25 5 25. 2 3 4 5 7 8 9 1 11 Figure 7. Temperatures of char siu during cooking and holding in a display window heated by infrared lamps (stablishment F). were put in these devices, temperatures fell to and remained within a range in which pathogenic bacteria could multiply rapidly. As can be seen in Fig. 7-9, the TABL 2. foods were near optimal temperatures for growth of common pathogenic food borne bacteria for a long while. At other times, as shown in Table 3 and in Fig. 5 and 6, cooked pork products were sometimes left at room temperature for several (as long as 18) hours. Under these conditions, there is an obvious potential for multiplication of bacteria. Stiles and Ng (12) showed that at 3 C (86 F) Bacillus cereus, C. perjringens, scherichia coli, Salmonella typhimurium, and S. aureus had a longer lag phase when inoculated into Chinese (so-called barbecued) pork tenderloin than when inoculated into commercially prepared, rotisserie-cooked chicken. The lag was 5 to 8 h, but after 2 to 22 h incubation, counts of these bacteria reached 1 5 to 1 9 During the present study, the foods stayed on display within a temperature range of 21 C (7 F) to 46 C (115 F) for periods of 5 to 8 h on one occasion and exceeded this time period on two other occasions. A few samples of pork were collected and tested for S. aureus, C. peifringens, and Salmonefla. Staphylococcus aureus was isolated from one sample of raw pork and from one sample of roast pork (Table 4). The cooked product was probably contaminated after cooking by workers who handled the pork or from equipment surfaces ltable 2). Clostridium perfringens was isolated from 3 to 14 samples of cooked pork. In all cases, only small numbers of these food borne pathogens were found (Table 4). Although Tiwari et al. (13) also found rather small numbers of S. aureus, C. peifringens, coliforms and fecal streptococci in cooked Chinese-prepared pork Prevalence of Staphylococcus aureus and Clostridium perfringens on equipment surfaces that contacted pork during in a restaurant and market. a quipment surface Restaurant (F)b Cutting board, 1 Cutting board, 2 Cleaver Steam table Stainless steel plate Hooks for roast duck Stainless steel pan Plastic pan TOTAL Market (G)b Cutting block 1 Cutting block 2 Cutting board Scale Metal tray Cleaver Meat-scale pan Metal skimmer Wiping cloth TOTAL GRAND TOTAL asalmonellae were not isolated from any of these samples. bstablishment identification. Staphylococcus au reus /8 8/9 8/17 Clostridium perfringens /8 7/9 7/17 JOURNAL OF FOOD PROTCTION, VOL. 45, APRIL 1982

TABL 3. Time-temperature exposures at geometric centers of cooked char siu during holding at room temperature or in refrigerators..j;:>. Holding unit/ Min Initial Final Min between Min between Potential for growth Product/ Temperature of temperature temperature 7-115 F 45-14 F of pathogenic (stablishment) (F) (F) (F) (21-46 Cl (7-6Cl food borne bacteria Charsiu (G) Walk-in 63 73 37 15 97 refrigerator I 24-6 Charsiu (A) Walk-in 415 182 38 28 117 refrigerator I 33-42 Cut of pork (G) Walk-in 63 8 37 55 16 a refrigerator I 24-6 t--. Charsiu (F) Walk-in 9 12 38 135 27 35-58 Charsiu (C) Room temperature/ 167 82 37 J 1:::1 67 ;;g OS Walk-in 82 38 :r32 5 3 t;j refrigerator I "-<: > (") 28-36 z :::J Charsiu (D) Room temperature Js7o 16 118 J33 r 95 }?; > < Walk-in - r refrigerator I 118 4 Y' 31-42 > Side of pork (G) Room temperature/ 75 165 138 5 ;:3 72-81 i= Charsiu - (A) Room temperature/ 123 167 72 >92 >16 >.. co 62-7 "' Charsiu (G) Room temperature/ 21 167 8 >155 >22 > 72-76 Charsiu () Room temperature/ 375 13 63 165 375 63-74 Charsiu () Room temperature/ 18 16 68 175 >16 73-77 Cut of pork (G) Glass cabinet 3 115 1 3 3 heated by infra- 85 12 12 6 6 red!amos and 24 185 94 155 195 255 95 87 255 255 1-92 Charsiu (G) Glass cabinet 338 13 9 >322 >338 heated by infra- =

HAZARD ANALYSS OF CHAR SIU 427 Figure 8. Temperatures of cooked char siu during holding at room temperature and in a glass-enclosed cabinet heated by a 15-watt infrared lamp, three 15-watt light bulbs and a!-watt light bulb (stablishment G). If) co ;c p "' 3 J5 "' <; e. Q "!"!" {' - Figure 9. Temperatures of roast pork during holding at room temperature in a glass-enclosed cabinet heated by a 15-watt infrared lamp. three 15-watt bulbs and one 1-watt light bulb (stablishment G). products, they observed that these organisms sometimes reached large numbers in these products after 22 h of incubation at 22 C (72 F). Cooling unused products Char siu was sometimes refrigerated within an hour or two after cooking, as shown in Table 3 and in Fig. 3 and 4. When this was done, little bacterial growth would be expected. Leftover char siu and roast pork were also refrigerated after holding on display (Table 3, Fig. 1). In these situations, some additional bacterial multiplication could occur, but in time would cease. Storage of a large quantity of leftover pork in a large container could, however, lead to considerable microbial growth. Reheating During reheating of chilled, precooked pork products, vegetative pathogens, if present, would have survived in the interiors (Table 1, Fig. 11). As shown by Bryan and Kilpatrick (3) and by Bryan and McKinley (4), meat products are often reheated to temperatures too low or for too short of a time to kill the large numbers of vegetative pathogenic bacteria that might have grown during periods of improper storage. Water activity Samples of roast pork and char siu were tested for water activity (aw> The aw of two samples of roast pork was.97 and.99. Results for char siu are presented in JOURNAL OF FOOD PROTCTION. VOL. 45, APRIL 1982

428 BRYANT AL. TABL 4. Prevalence ofstaphylococcus aureus and Clostridium perfringens in pork during various stages of processing. a Product/ Stage of Staphylococcusb Clostridiumb (stablishment) au reus Raw Charsiu (F) Raw, marinated 2 <1 Raw pork (G) Raw, swab Neg. Neg. TOTAL 112 12 Cooked Spare ribs (F) After cooking <1 <1 Charsiu (F) During display <1 <1 (in window) Charsiu (F) During display <1 <1 (in window) (Hobbs 4) Roast pork (G) During display <1 <1 (in cabinet) Roast pork (G) During display <1 <1 (in cabinet) Charsiu (F) Steam table <1 <1 Charsiu (F) Before refrigeration <1 <1 Charsiu (F) Before refrigeration <1 <1 Pot roast pork (F) After cooling <1 <1 Char siu (F) After cooling <1 <1 Spare ribs (F) After cooling <1 <1 Ground char siu (F) After cooling <1 <1 (for fried rice) Charsiu (G) After cooling <1 <1 Roast pork (G) After cooling <1 <1 TOTAL POSITIV 1/14 3/14 a salmonella was not isolated from any of the samples. b<lo indicates that less than 1 S. aureus or C. perfringens were present. buts. aureus or C. perfringens was isolated. 125 w..: 1 SIU ;;-' 75 ::J ::; "' c; Q; 5 2 Cl. Refr:gercror o;r "' 25!- 2 3 Figure 1. Temperatures ofa strip Q(char siu during cooling in a walk-in refrigerator (stablishment F). Table 5. The aw of center slices of char siu ranged from.89 to.97, with a median of.95. Trimmings of the surface had aw values that ranged from.88 to.97, with a median of.93. Diced pieces of char siu, which had been at room temperature for a few hours and were to be used in soup, had an aw value of.86. Growth of common gram-negative spoilage bacteria is inhibited at aw values less than.98 (9). Therefore, spoilage of char siu would not likely be caused by gram-negative bacteria such as Pseudomonas spp. Few pathogenic foodborne bacteria would be expected to multiply at aw values below.95 (9). Some strains of S. aureus could multiply, but there has been no evidence of enterotoxin production when the aw value was below. 92 (14). Some pieces of char siu would have a low enough aw to retard or perhaps even prevent the growth of foodborne pathogens but not under all situations prevent "' Cl. 5 45 4 U..: 35 3 25 2 15 1 5... Pork ribs /--- / - --S..o s/u --7-- r---------- 1 /./t Cut ot pork Out ot oven 5 1Q 15 2 25 25 225 2 175 u 125 1 Minutes Figure ll. Temperatures at geometric centers of cooked ribs, char siu, and cut of pork during reheating in an oven (stablishment G). 75 5 25 Q).._ :J -.._ Q) a. JOURNAL OF FOOD PROTCTION. VOL. 45. APRIL 1982

HAZARD ANALYSS OF CANTONS FOODS 421 TABL 4. Bacterial counts of Chinese foods after being held at room temperature and/ or refrigerated. Description/ (stablishment} ggfoo yung cooled at room temperature for approximately 5 to 6 h and then refrigerated. (C) ggfoo yung refrigerated overnight,left at room temperature for approximately 8 h and then refrigerated. (C) Bacillus cereus <1 X 1 1 <1 X 11 Aerobic colony count (3 6.8 X 1 4 4. X 1 3 ACKNOWLDGMNTS We thank the following persons for their assistance in this study: Harold Matsuura, Tsutomu Kubota, Tadashi Ogata, Frank Sakato, Beatrice Sakai of the Hawaii State Department of Health; Norma Christopherson and Mohammad Ayaz, Washington State Department of Social and Health Services; and to numerous persons who managed and worked in the establishments surveyed. RFRNCS ggfoo yung left at room temperature for approximately 8 h and then refrigerated. (C) ggfoo yung left at room temperature for approximately Sh. () ggfoo yung left at room temperature for over 2 h. () Batter-fried pork held at room temperature for over 8 h. (C) Pork ribs held at room temperature for over 8 h. () Batter-fried pork held at room temperature for 2 h. () gg roll, uncooked, refrigerated for 2 days. () gg roll held at room temperature 8 to 1 h. () 1 X 1 2 1 X 1 2 2.7 X los <1 X 1 1 <1 X 1 1 L9x 1 4 <1 X 1Q1 1 X 1 1 1. X 15 1.2 X 1Q6 3.5 X 1Q8 1.8 X 1Q4 2.8 X 1 7 1.2 X 1 6 1. Bryan, F. L., K. A. Seabolt, R. W. Peterson, and L. M. Roberts. 1978. Time-temperature observations of food and equipment in airline catering operations. J. Food Prot. 41:8-92. 2. Bryan, F. L., C. A. Bartleson, and N. Christopherson. 1981. Hazard analysis, in reference to Bacillus cereus, of boiled and fried rice in Cantonese-style restaurants. J. Food Prot. 44:5-512. 3. Gilbert, R. J. 1979. Bacillus cereus gastroenteritis. In H. Reimann and F. L. Bryan (eds.} Foodborne infections and intoxications, 2nd ed. Academic Press, New York. 4. International Commission on Microbiological Specifications for Foods. 198. Microbial ecology of foods. vol. 1. Factors affecting life and death of microorganisms. Academic Press, New York. 5. Speck, M. L. (ed.) 1976. Compendium of methods for the microbiological examination of foods. American Public Health Association, Washington, DC. 6. Troller. J. A. 1975. Influence of water activity on growth and enterotoxin formation by Staphylococcus aureus in foods. J. Food Sci. 4:82-84. 7. Troller, J. A., and J. H. B. Christian. 1978. Water activity and food. Academic Press, New York. 8. U.S. Department of Health, ducation, and Welfare. 1976. Food service sanitation manual. U.S. Government Printing Office, Washington, DC. 9. U.S. Department of Health, ducation, and Welfare. 1979. Foodborne and waterborne disease outbreaks. Annual summary 1977. Center for Disease Control, Atlanta, Georgia. JOURNAL OF FOOD PROTCTION, VOL. 45, APRIL 1982