422

Journal ofFood Protection, Vol. 45, No.5, Pages 422-429 (Aprill982) Copyright© International Association of Milk, Food, and Environmental Sanitarians

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

FRANKL. BRYAN I*, CHARLES A. BARTLESON2, MITSUTO SUGI3, BEATRICE SAKAI3, LLOYD MIYASHIR03, STEVEN TSUTSUMI3 a.nd CLIFFORD CHUN3 U.S. Department a;f'Health and Human Services, Public Health Service, Centers for Disease Control, Washington State Department ofSocial and Health Services. and Hawaii State Department a;f'Health Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021

(Received for publication March 25, 1981 l

ABSTRACT pork (ham) and barbecued pork that have been prepared in foodservice establishments other than Chinese Evaluations of time-temperature exposure of each stage of restaurants have often been identified as vehicles of the preparation of char siu (marinated roast pork) were made at six Chinese restaurants and a market. These evaluations were foodborne illness <;!,5,12,13). Char siu, which ts also made of roast pork at the market. Samples of these marinated roast pork but is often referred to as products at the various stages of preparation and swabs of barbecued pork, prepared in Chinese restaurants has equipment surfaces that the pork touched during preparation only rarely been incriminated (10,15). Yet, because this were tested for Clostridium perfringens, Salmonella and product is quite popular and consequently is kept Staphylococcus aureus. The water activity of other samples was available for serving, it often remains for long periods of also determined. Temperatures attained at the geometric time within a temperature range that is suitable for center of these pork products during roasting in ovens or after growth of food borne pathogenic bacteria. Whether this cooking ceased were such that vegetative pathogenic food borne apparent failure to be a vehicle in foodborne disease bacteria should have been killed, if present. The cooked outbreaks could be real or a result of the lack of reports products were often displayed in warming cabinets or window or incomplete investigations has not been examined. The counters at which time their temperatures were within a range that would permit rapid bacterial growth for several hours. purpose of this investigation was to (a) ascertain Reheating of leftover pork was inadequate to destroy hazardous operations associated with the preparation pathogenic microorganisms that grew or toxins that were and storage of pork products in several Chinese produced during storage. The water activity of char siu was restaurants and in a Chinese market, (b) to relate these frequently at a level that would increase the bacterial lag phase findings to the water activity of the product, and (c) to and slow the rate of growth of pathogenic bacteria from identify critical control points of typical preparation optimum. A few samples of char siu were contaminated by low activities. numbers of C. perfringens and a sample of raw and roast pork with S. aureus. There were opportunities for contamination of MATERIALS AND METHODS cooked pork products during preparation, particularly at the Operations market. Critical control points for these operations--handling Char siu is cut into rectangular strips approximately 3 em after cooking, hot-holding, cooling and reheating--are given (1.2 in) by 6 em (2.4 in) and 20 to SO em (8 to 20 in) long that is along with measures for controlling and monitoring these marinated in a solution of sugar. salt, spices, and red dye. It is points. 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 Foods prepared in Chinese restaurants have been (<1 em thick) for use in won ton soup. fried rice or other dishes. reported as vehicles of foodborne disease outbreaks Sides of fresh hog carcasses were left overnight at room temperature. (6,7.10,12,13). Boiled rice and have often been Salt was rubbed over the surface and into cuts made in the flesh. After incriminated as vehicles, but, in many other investiga­ roasting in an oven. the sides were cut into chunks of roast pork and stored in glass cabinets until sold. tions, specific vehicles have not been identified. Cured Operations involved in preparing char siu were evaluated in six restaurants (A. B. C. D. E. F) and at a market (G) that were located 1 U.S. Department a;l Health and Human Services. Public Health in either the states of Hawaii or Washington. Operations for preparing Service, Centers for Disease Control. Atlanta. Georgia 30333. the cuts of roast pork were evaluated at the market. 2Washington State Department a;( Social and Health SeT'I!ices, O{vmpia, Washington 98504. i\1 easureme,1ts 'Hawaii State Department ofHealth. Honolulu. Hawaii 96801. Water activity (aw) was evaluated with an electric hygrometer.

JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982 HAZARD ANALYSES OF CHAR SIU 423

Specifications for this instrument have been published (6). Recordings cooking are summarized in Table 1 and examples are were usually made at 25 C (77 F), however, a few recordings were made illustrated in Fig. 3-7. The highest temperatures attained at other temperatures. Several samples were frozen and thawed before at the geometric centers of pieces of char siu ranged from analysis for~- Time-temperature measurements were obtained with thermocouples 61 C (142 F) to 91 C (195 F). Internal temperatures of the and recorded on a recording potentiometer. Specifications for this roast pork reached 74 C (166 F) and 81 C (178 F). The instrument have been published 0-6). Necdle·point thermocouples temperatures rose as much as 4 C (7 F) after cooking were inserted into the meat so that the sensing end was located near the ceased. According to established D-values for various geometric center. Welded-junction thermocouples were used to measure air temperatures. pathogenic bacteria in similar substrates (1,8), the time-temperature values attained in these products Laboratory should have killed most vegetative pathogenic foodborne Samples for laboratory analysis were taken as described by Bryan et al. (4.6). bacteria that might have been present. Laboratory procedures for the isolation of Clostridium perfringens, Salmonella and Staphylococcus aureus are described in the Bacteriological Analytical Manual (} 6). Oven a;r RESULTS AND DISCUSSION Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021 Storage ofraw products Temperature changes in a side of raw pork (at the center of a thigh) held overnight at room temperature are Out of oven and to refrigerator shown in Fig. 1. The temperatures were such that * psychrotrophic and mesophilic microorganisms could have multiplied for several hours. ---165°F -- 150° F. 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.

Hours 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).

Hours 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).

Handling cooked products Hours Cooked pork products were often handled by workers Figure 2. Temperatures of0.6-lb strip of char siu marinating who had previously handled raw meat or raw poultry. in a walk· in refrigerator (F;stablishment F). The cooked products were chopped and sliced on cutting boards with cleavers and knives that were also used for Cooking other purposes. The cooked pork could easily have Time-temperature exposures of char siu during become contaminated during this operations because S.

JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982 424 BRYANETAL.

~~~IT 175 325 ~ / :Oven air 150

lL ~~~J~.250 . 125 0 . . Q) 225 . 0 0 ~ .2 200 . 1100 ~ 0 . I ~ Q; 175 75 ~ 150j'_ ----150° F------65socl l Char siu E r-- 125 50 100 ~ 75 25 Room air 50

25 0 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021

0~,,-,,-,-,-,,-,-,-,,-"-,~1 0 2 3 4 56 7 8 9101 11213141516171819 Hours Figure 5. Temperatures at geometric center of char siu during cooking and during subsequent holding at room temperature (Establishment E).

500 475 250 450 Oven a1r 225 425 400 375 350 r~7050

lL 325 0 300 I S1de 1 t150 ~ ~ out of oven Q) 2 275

0 • Pork s 1 de 1, S1de 1 .... d 125 250 2 .2 0:; Char stu ( center of cutdup . Q. 225 ~~~eat ~ oolfllflOOOO-VlN t-- E ;emoved th1gh meat ~noved oven 100 E -,olflOO-.D-.D-.D0\"<1" -.D 200 rom ~ven to the ._ i OJ 175 market ; I- '"' '~ • [-75 ------150 150o F--.~- -~,~~~=:~/,(;~$;~- =~ -, 65 soc! SO 125 ~ -==.:::::--. Porks1deZ,centerr 100 ----'------=-·- -·of shoulder meat 1 • Center of t ' 25 75 t Meat removed Char stu Side 2 50 from oven and 1nto oven 25 holes poked 0 through sk1n 0 0 4 Hours Figure 6. Temperatures ofpork sides and marinated strips of char siu during cooking and room-temperature storage (Establishment G). aureus and C. perfringens were frequently isolated from swab samples of utensils, equipment or cloths in the 1:11) :::: :::: market, but they were not isolated from swab samples ·- 4- ·.p ::;; 0 ~ 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

JOURNAL OF FOOD PROTECTION. VOL. 45. APRIL 1982 HAZARD ANALYSES OF CHAR SIU 425

4758 foods were near optimal temperatures for growth of 450 .··. ·• common pathogenic food borne bacteria for a long while. 225 425 :•.•• At other times, as shown in Table 3 and in Fig. 5 and 6, 400 •• Oven air cooked pork products were sometimes left at room 200 375 temperature for several (as long as 18) hours. Under these conditions, there is an obvious potential for 350. 175 multiplication of bacteria. ~)25 . Stiles and Ng (12) showed that at 30 C (86 F) Bacillus ~ 300. 150 cereus, C. perjringens, Escherichia coli, Salmonella u e 275 0 ::::l typhimurium, and S. aureus had a longer lag phase when 125 Q) 0 250 "'- inoculated into Chinese (so-called barbecued) pork ,._ ::::l :g_ 225 +- tenderloin than when inoculated into commercially 100 ,._0 E 200 Q) prepared, rotisserie-cooked chicken. The lag was 5 to Q) a. r:- 175 E 8 h, but after 20 to 22 h incubation, counts of these 75 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021 5 9 150 ~ bacteria reached 10 to 10 • During the present study, the foods stayed on display within a temperature range of 125 50 21 C (70 F) to 46 C (115 F) for periods of 5 to 8 h on one 100 occasion and exceeded this time period on two other Display area air 25 75 occasions. 50 A few samples of pork were collected and tested for S. 25 0 aureus, C. peifringens, and Salmonefla. Staphylococcus 0. aureus was isolated from one sample of raw pork and 0 2 3 4 5 7 8 9 10 11 from one sample of roast pork (Table 4). The cooked Hours product was probably contaminated after cooking by Figure 7. Temperatures of char siu during cooking and holding in a display window heated by infrared lamps workers who handled the pork or from equipment (Establishment F). 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 were put in these devices, temperatures fell to and (Table 4). Although Tiwari et al. (13) also found rather remained within a range in which pathogenic bacteria small numbers of S. aureus, C. peifringens, coliforms could multiply rapidly. As can be seen in Fig. 7-9, the and fecal streptococci in cooked Chinese-prepared pork TABLE 2. Prevalence of Staphylococcus aureus and Clostridium perfringens on equipment surfaces that contacted pork during in a restaurant and market. a

Staphylococcus Clostridium Equipment surface au reus perfringens 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 0/8 0/8 Market (G)b Cutting block 1 Cutting block 2 + + Cutting board + Scale + + Metal tray + + Cleaver + + Meat-scale pan + + Metal skimmer + + Wiping cloth + + TOTAL 8/9 7/9 GRAND TOTAL 8/17 7/17 asalmonellae were not isolated from any of these samples. bEstablishment identification.

JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982 .j;:>. TABLE 3. Time-temperature exposures at geometric centers of cooked char siu during holding at room temperature or in refrigerators. ~

Holding unit/ Min Initial Final Min between Min between Potential for growth Product/ Temperature of temperature temperature 70-115 F 45-140 F of pathogenic (Establishment) (F) (F) (F) (21-46 Cl (7-60Cl food borne bacteria Charsiu (G) Walk-in 630 73 37 15 97 refrigerator I 24-60 Charsiu (A) Walk-in 415 182 38 28 117 refrigerator I 33-42 Cut of pork (G) Walk-in 630 80 37 55 160 a refrigerator I ~ 24-60 t--.~ Charsiu (F) Walk-in 900 102 38 135 270 + ~ 35-58 ~ 0 Charsiu (C) Room temperature/ 167 82 1:::1 67 ;;g ~370 OS Walk-in 38 :r32 0 ~ 82 5 3 = refrigerator I J "-<: t;j > (") 28-36 z :::J 0 Charsiu (D) Room temperature 160 118 ~ ?; > Js7o 95 r < Walk-in 118 40 ~ J330 } 0 - r refrigerator I ~ Y' 31-42 > Side of pork (G) Room temperature/ 75 165 138 0 5 ;:3 72-81 i= Charsiu (A) Room temperature/ 123 167 72 >92 >106 >+ -co..0 "' 62-70 Charsiu (G) Room temperature/ 210 167 80 >155 >202 >++ 72-76 Charsiu (E) Room temperature/ 375 130 63 165 375 +++ 63-74 Charsiu (E) Room temperature/ 1080 160 68 175 >1060 +++ 73-77 Cut of pork (G) Glass cabinet 30 115 100 30 30 heated by infra- 85 120 102 60 60 red !amos and 240 185 94 155 195 ++ 255 95 87 255 255 ++++ 10-92 Charsiu (G) Glass cabinet 338 130 90 >322 >338 ++++

heated by infra- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021 September 28 on guest by http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf from Downloaded HAZARD ANALYSES OF CHAR SIU 427

Hours Figure 8. Temperatures ofcooked char siu during holding at room temperature and in a glass-enclosed cabinet heated by a 150-watt infrared lamp, three 150-watt light bulbs and a !00-watt light bulb (Establishment G). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021

If) co ;c p ~ "'3 "' 0 J5 <; e 0. "Q E E !" !"

{' Hours 0 Figure 9. Temperatures ofroast pork during holding at room - temperature in a glass-enclosed cabinet heated by a 150-watt infrared lamp. three 150-watt bulbs and one 100-watt light bulb (Establishment 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. 10). In these situations, some additional bacterial multiplica­ tion 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 0.97 and 0.99. Results for char siu are presented in

JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982 428 BRYANET AL.

TABLE 4. Prevalence ofStaphylococcus aureus and Clostridium perfringens in pork during various stages ofprocessing. a

Product/ Stage of Staphylococcusb Clostridiumb (Establishment) au reus Raw Charsiu (F) Raw, marinated 20 <10 Raw pork (G) Raw, swab Neg. Neg. TOTAL 112 012 Cooked Spare (F) After cooking <10 <10 Charsiu (F) During display <10 <10 (in window) Charsiu (F) During display <10 <10+ (in window) (Hobbs 4) Roast pork (G) During display <10 <10 (in cabinet) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021 Roast pork (G) During display <10+ <10 (in cabinet) Charsiu (F) Steam table <10 <10 Charsiu (F) Before refrigeration <10 <10+ Charsiu (F) Before refrigeration <10 <10+ Pot roast pork (F) After cooling <10 <10 Char siu (F) After cooling <10 <10 Spare ribs (F) After cooling <10 <10 Ground char siu (F) After cooling <10 <10 (for fried rice) Charsiu (G) After cooling <10 <10 Roast pork (G) After cooling <10 <10 TOTAL POSITIVE 1/14 3/14 a salmonella was not isolated from any of the samples. b

125

w..: 100 500 0 SIU ;;-' 250 ~ ::J 75 ::;"' ... c; 450 Q; 50 2 225 Cl. "'Cl. E Refr:gercror o;r E 25 !-"' ~ 400 200 0 0 2 3 U..: 350 175 u Hours 0 0 Figure 10. Temperatures ofa strip Q(char siu during cooling 300 Q).._ in a walk-in refrigerator (Establishment F). :J +- 0 250 125 .._ Table 5. The aw of center slices of char siu ranged from Q) 0.89 to 0.97, with a median of 0.95. Trimmings of the a. __ _ 100 E surface had aw values that ranged from 0.88 to 0.97, with 200 /--- a median of 0.93. Diced pieces of char siu, which had ~ / ·-·--S..~o~ s/u 75 been at room temperature for a few hours and were to be 150 --7-- ~r------used in , had an aw value of0.86. 1 /./t Cut ot pork 50 Growth of common gram-negative spoilage bacteria is 100 inhibited at aw values less than 0.98 (9). Therefore, ~· Out ot 25 oven spoilage of char siu would not likely be caused by 50 gram-negative bacteria such as Pseudomonas spp. Few 0 pathogenic foodborne bacteria would be expected to multiply at aw values below 0.95 (9). Some strains of S. aureus could multiply, but there has been no evidence of 0 5 1Q 15 20 25 enterotoxin production when the aw value was below 0. 92 Minutes (14). Some pieces of char siu would have a low enough aw Figure ll. Temperatures at geometric centers of cooked ribs, to retard or perhaps even prevent the growth of char siu, and cut of pork during reheating in an oven foodborne pathogens but not under all situations prevent (Establishment G).

JOURNAL OF FOOD PROTECTION. VOL. 45. APRIL 1982 HAZARD ANALYSES OF FOODS 421

TABLE 4. Bacterial counts of Chinese foods after being held ACKNOWLEDGMENTS at room temperature and/or refrigerated.

Description/ Bacillus Aerobic colony We thank the following persons for their assistance in this (Establishment} cereus count (30 study: Harold Matsuura, Tsutomu Kubota, Tadashi Ogata, Frank Sakato, Beatrice Sakai of the Hawaii State Department of Health; Eggfoo yung cooled at room <1 X 101 6.8 X 104 temperature for approximately Norma Christopherson and Mohammad Ayaz, Washington State 5 to 6 h and then refrigerated. Department of Social and Health Services; and to numerous persons who managed and worked in the establishments surveyed. (C)

Eggfoo yung refrigerated over­ <1 X 101 4.0 X 103 night,left at room temperature for approximately 8 h and then REFERENCES refrigerated. (C)

Eggfoo yung left at room 1 X 102 1.0 X 105 1. Bryan, F. L., K. A. Seabolt, R. W. Peterson, and L. M. Roberts. temperature for approximately Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/5/422/1653753/0362-028x-45_5_422.pdf by guest on 28 September 2021 1978. Time-temperature observations of food and equipment in 8 h and then refrigerated. (C) airline catering operations. J. Food Prot. 41:80-92. 2. Bryan, F. L., C. A. Bartleson, and N. Christopherson. 1981. Hazard Eggfoo yung left at room 1 X 102 1.2 X 1Q6 analysis, in reference to Bacillus cereus, of boiled and fried rice in temperature for approximately Cantonese-style restaurants. J. Food Prot. 44:500-512. Sh. (E) 3. Gilbert, R. J. 1979. Bacillus cereus gastroenteritis. In H. Reimann and F. L. Bryan (eds.} Foodborne infections and intoxications, 2nd Eggfoo yung left at room 2.7 X lOS 3.5 X 1Q8 ed. Academic Press, New York. temperature for over 20 h. (E) 4. International Commission on Microbiological Specifications for Foods. 1980. Microbial ecology of foods. vol. 1. Factors affecting life and death of microorganisms. Academic Press, New York. Batter-fried pork held at X 1 <1 10 1.8 X 1Q4 5. Speck, M. L. (ed.) 1976. Compendium of methods for the room temperature for over 8 h. microbiological examination of foods. American Public Health (C) Association, Washington, DC. 6. Troller. J. A. 1975. Influence of water activity on growth and Pork ribs held at room <1 X 101 enterotoxin formation by Staphylococcus aureus in foods. J. Food temperature for over 8 h. (E) Sci. 40:802-804. 7. Troller, J. A., and J. H. B. Christian. 1978. Water activity and food. 4 Academic Press, New York. Batter-fried pork held at L9x 10 2.8 X 107 room temperature for 20 h. (E) 8. U.S. Department of Health, Education, and Welfare. 1976. Food service sanitation manual. U.S. Government Printing Office, Washington, DC. Egg roll, uncooked, refrigerated <1 X 1Q1 9. U.S. Department of Health, Education, and Welfare. 1979. for 2 days. (E) Foodborne and waterborne disease outbreaks. Annual summary 1977. Center for Disease Control, Atlanta, Georgia. 1 Egg roll held at room 1 X 10 1.2 X 106 temperature 8 to 10 h. (E)

JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982