445 Journal o_ffood Protection, Vol. 45, No.5, Pages 445-449 f.apri/1982) Copvright International Association of Milk, Food, and Environmental Sanitarians Hazard Analyses of Duck in Chinese Restaurants FRANKL. BRYAN I., MITSUTO SUGI2, LLOYD MIYASHIR2, STEVEN TSUTSUMI2 and CHARLES A. BARTLESON a U.S. Department ofhealth and Human Services, Public Health Service, Centers for Disease Control; Hawaii State Department o.fhealth; and Washington Department of Health and Social Services (Received for publication March 23, 1981) ABSTRACT Time-temperature exposures and water activity values were measured during the preparation and storage of Chinese-style duck products. Frozen ducks were usually thawed at room temperature and remained at room temperature for several hours thereafter. During cooking or during the post-oven temperature rise period, the temperatures at the geometric centers of the ducks exceeded 94 C (21 F). Cooked ducks were subjected to cross-contamination when they were chopped or cut up on cutting boards. Cooked ducks were held for several hours at bacteria-incubating temperatures while they were on display in cabinets or on counters. Leftover cooked ducks cooled rather rapidly during refrigerated storage. When they were reheated, their internal temperatures did not rise to levels lethal to vegetative pathogenic bacteria. Water activity values of cooked duck ranged from.87 to.99. Critical control points of the operations were the cutting and chopping of cooked ducks, storage of ducks during display for sale and reheating leftover ducks. Recommendations for control are: (1) to hold cooked ducks at 55 C (131 F) or above, (2) cool unsold cooked ducks rapidly, (3) reheat leftover ducks to internal temperatures of 71-74 C (16-165 F), and (4) minimize opportunities of contamination from equipment surfaces and workers' hands. In recent years, foods, particularly boiled rice and fried rice, that are prepared in Chinese restaurants have been implicated as vehicles of foodborne disease outbreaks (3,4). Duck, which is popular in Chinese restaurants, is seldom implicated as a vehicle of disease even though it is often displayed at room or other bacteria-incubating temperatures. This seems strange because other poultry products, particularly turkey and chicken, are frequently implicated as vehicles in outbreaks of foodborne disease (1). This investigation 1 U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control, Atlanta, Georgia 3333. 2 Hawaii State Department of Health, Honolulu, Hawaii 9681. 3 Washington Department of Health and Social Services, Oympia, Washington 9854. was made to ascertain hazards that are associated with ducks prepared and stored in the traditional Chinese manner. Operations MATERIALS AJ'to'D METHODS Four establishments were investigated: three restaurants (identified as A, B and F) and a market (identified as G). Preparation of duck varied somewhat among these establishments. In general, however, Peking duck was prepared by thawing frozen Long Island duck carcasses at room temperature overnight. After they had thawed, the carcasses were seasoned with sugar, salt, monosodium glutamate and spices; sometimes the ducks were stuffed with parsley and green onions. They were then immersed into hot water for several seconds after which they were dipped into a hot mixture of water, vinegar and red dye. Next they were inflated with air from a hose and refrigerated overnight. The following morning the ducks were cooked in an oven then usually displayed on counters by windows or in glass cabinets until they were sold. The cabinets and counter area were heated by infrared lamps, incandescent light bulbs or a combination of the two. In general, pressed duck was thawed overnight in a walk-in refrigerator, then marinated in soy sauce and herbs, usually overnight in the refrigerator, and cooked the next day. The ducks were skinned, then cooled in the refrigerator. Following cooling they were boned, the meat molded into patties, and the patties were wrapped in the skin. The wrapped meat was then pressed. The pressed duck was refrigerated until ordered, at which time it was reheated in oil in a wok and sliced for serving. Other style ducks were roasted in ovens, then held at room temperature until refrigerated or sold. Ducks that were not sold were refrigerated overnight and reheated the next day. Measurements Water activity was measured with an electric hygrometer as previously described (3). Temperature measurements were taken by thermocouples and recorded on a recording potentiometer as described previously (2,3). Needle-point thermocouples were inserted into the thickest portions of breasts, legs or thighs of the ducks. Weldedjunction thermocouples were used to measure air temperatures. Surface temperatures were measured by button-type thermocouples, the sensor being attached by wires around the carcass. RESULTS AND DISCUSSION During thawing of raw, frozen duck carcasses and during subsequent holding at room temperature, JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982
446 BRYANETAL. surfaces of the carcasses were warm enough for sufficient time to permit bacterial multiplication. An example of this is shown in Fig.1 where the surface temperature was at or above 21 C (7 F) for 7 h. The effect of heat on the duck skin during dipping was not evaluated. The period of immersion in the acidic mixture was quite short, but the hot water and vinegar could have reduced the microbial population of surface flora. The inflation of the carcass with compressed air may have affected the distribution of salts throughout the carcass which could have altered the water activity of the duck. After the carcasses had been dipped and inflated, they were refrigerated and their internal temperatures dropped to 7 C (45 F) within 4 h, as shown in Fig. 2. pathogenic foodborne bacteria but not sufficient to have killed all spores of Clostridium peifringens. Examples of a temperature curve during cooking and reheating of a cooked Peking duck are shown in Fig. 3 and 4. Unless cooked ducks were sold whole, they were either chopped or cut on cutting boards. Cutting boards, knives and deavers were occasiona11y wiped with rags but were usualjy not washed until the end of the day's operation and were obviously implements for cross-contamination. While cooked ducks were held on display in Establishments F and G, their temperatures dropped in about 1.25 h to a range in which pathogenic foodborne bacteria could multiply. They stayed within that range until sold or refrigerated for the night (Table 2, Fig. 4). 8 _...------- --------- - 7 _,..- Room temperature i 61., i 5] Surface 2 (.) j ::11 2 1 LL-r------.-.-.-.-.-.-. 3 4 5 6 7 8 9 1 11 12 13 14 15 16 f-lours Figure 1. Surface temperatures of 1.9 kg (4.25 lb) Long Island duck during holding at room temperature after thawing (Jl:stablishment F). -1 2 LL 6 '... ' '... -- -----.------------ Refrigerator air (.) 1 <lj... :::) +- e <lj OE Minutes Figure 3. Temperatures at thickest portion of breast of 1.9 kg (4.25lb) Peking duck during cooking and reheating in an oven. (Jl:stablishment F). wtn::ow c sp:ay 1 1 2 3 4 Hours Figure 2. Temperatures of 1.9 kg (4.25 lb) raw Peking duck during storage in a reach in refrigerator (Jl:stablishment F). During cooking, internal temperatures of the duck meat reached 92 C to 96 C (197 F to 24 F) and rose to the range of 95 C to 97 C (23 F to 26 F) during the post-oven interval. As shown in Table 1, time-temperature exposures were sufficient to have killed vegetative -1 75 l;- p e ::> " 5 -e a. "' a. E E F' 25 4 8 9 Hours 25 I-- "' Figure 4. Temperatures at thickest portion of breast of 1.9 kg (4.25 lb) Peking duck during cooking and holding in a display window heated by infrared lamps (Jl:stablishmentF). JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982
-'Z I tr1 ::e tr1 Vl ;;! c:: t --.1 TABLE I. Time-temperature exposures of internal regions of breasts or legs of ducks during cooking and reheating in ovens. Highest temperature Highest temperature Minutes at Minutes at Minutes at Minutes at Minutes of ("F) reached ( F) reached during or above or above or above or above Establishment heating during heating post-heating rise 13 F (54.4 C) 14 F (6 C) 15 F (65.5 C) 165 F (73.9 C) 51 197 24 18 16 14 1 F 65 2 2 so 48 46 41 G 74 22 23 39 35 32 27 F 78 24 25 17 92 78 6 A 76 24 26 3 28 25 21 F 26a 143 4 1 F a Reheating. C5 t-- \::) :::J < r.1:> Y'., > ::e r: TABLE 2. Time-temperature exposures of internal regions of cooked ducks during holding in display areas, at room temperature or in refrigerators. Holding unit/ F temperature range Display window heated by infrared lamps/74-93 Enclosed cabinet heated by infrared lamps and light bulbs/83-93 Room temperature/ 65-74 Walk-in refrigerator/ 33-42 Room temperature/ 67 Walk-in refrigerator/ 32-42 Initial Final Minutes between Minutes between Potential for growth Minutes of temperature temperature 7F-11SF 45F-14F of pathogenic holding ("F) reached ("F) reached (21 C 46 C) (7C- 6C) food borne bacteria Establishment 465 23 9 >378 >413 F 45 36 TI7l _ill} :1 4 42 >84 2 2 23 9 usa acooling in progress when temperature monitoring began. 74 92 9 9 42 74 44 >367 >45 >277 > 315 >) >:J 3 > 12 185 >1 >;:] >385 25 27 >29 >63 =:J+ I +I- G G A B
448 BRYANETAL. Combinations of storage at room temperature and refrigerated storage, as encountered in Establishments A and B, also resulted in time-temperature exposures that could have permitted the multiplication of bacteria in or on cooked ducks (fable 2). Data in Table 2 show that some cooked, whole ducks were held within temperature range (7 C to 6 C; 45 F to 14 F) for more than 4 h which exceeds recommendations of the Food Service Sanitation Manual (8). Internal temperatures of the cooked and chilled ducks did not always reach levels during reheating that would have killed vegetative pathogenic foodborne bacteria (Table 2, Fig. 3). A few samples of duck were tested for water activity (aw) Results are shown in Table 3. Four of the samples had aw values of.98 or above; these should permit rapid multiplication of microorganisms. Four other samples had aw values of.97 which would have allowed multiplication of most foodborne pathogenic bacteria, but with increased lag at a slower rate. The lower aw values observed would have prolonged multiplication even more and prevented entirely the growth of certain microorganisms. Most gram-negative spoilage bacteria do not multiply at aw values of. 98 or less (5). Few food borne pathogens multiply at aw values of.95 or less, and Staphylococcus aureus has not been shown to produce enterotoxin at aw values of less than.92, although this organism has grown at an aw value as low as.83 (5). The comparatively low aw could be a factor influencing the observed lag of 5 to 8 h before Bacillus cereus. C. peifringens. Escherichia coli. Salmonella typhimurium and S. aureus multiplied in Chinese barbecued duck at 3 C (86 F) reported in the study by Stiles and Ng (6). In that instance, organisms finally did reach large numbers TABLE 3. Water activity of samples of cooked duck. Description Sample No. tested of Center llw Temperature product slice Skin Pressed duck 1.91 22/72 A 1.87 22/72 A Oven-baked 2.99 25/77 A (barbecued) duck 3.98 25/77 B 2.97 25177 A 3.97 25/77 B 4.88 22/72 A Peking duck 5 5.99 18/65 F 6.98 25/77 F 6.97 25177 F 7.97 25/77 F 8.94 27/8 F 7.92 25/77 F 8.92 25177 F a (13 to 19), but only after 2 to 22 h of incubation at this temperature. Such aw values could also account for the results of Tiwari et al. (7). They found rather small numbers of S. aureus and certain indicator organisms on samples of cooked duck from Chinese restaurants, but there were substantial increases in numbers after 2 h of incubation at 22 C (72 F). CONCLUSIONS There is a potential for contamination of cooked ducks in many Chinese restaurants and markets and for considerable abuse of time-temperature exposures after cooking. Ducks are sometimes contaminated with pathogens when they arrive in the kitchen and bacterial multiplication can occur during room-temperature storage of thawed ducks. Many of these bacteria, however, would be killed during cooking. Therefore, the critical control points ofthe preparation of ducks are the operations that follow cooking. Particular care must be given to minimize contamination from hands, cleavers, knives, cutting boards, table tops, wiping cloths, storage pans and workers' hands during handling and preparing cooked ducks. Storage of cooked ducks at room temperature or in display counters or cabinets is the problem that causes most concern. Unless the water activity of cooked ducks can be shown conclusively to be sufficiently low, which it frequently cannot, the following procedures should be used: (a) temperatures to which cooked ducks are exposed during hot storage should be at or above 55 C (131 F) throughout; (b) cooked ducks should be cooled after cooking or hot-holding so that their internal temperatures fall rapidly (within 2 h) to 21 C (7 F) and then continue to cool (within another 4 h) to 7 C (45 F) or below; (c) more care should be given to reheating previously prepared or leftover duck to temperatures of 71 C to 74 C (16 F to 165 F) at the geometric center of the thickest region of the duck so that common vegetative pathogenic bacteria, which may have contaminated the ducks or which may have multiplied on or in them during storage, are certain to be killed; and (d) a monitoring system should be devised to ensure that the above recommendations are continually carried out. ACKNOWLEDGMENTS Thanks is given to the following persons for their assistance in this studv: Harold Matsuura. Tsutomu Kubota, Tadashi Ogata and Frank Sakto of the Hawaii State Depanment of Health; to Norma Christopherson and Muhamed Ayez, Washington Depanment of Social and Health Services; and to numerous persons who managed and worked in the establishments surveyed. Thanks is also given to Dr. Hilliard Pivniek. Health Protection Braneh, Health and Welfare Canada, Ottawa. for reviewing the manuscript. JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982
DUCK IN CHINESE RESTAURANTS 449 REFERENCES 1. Bryan, F. L. 198. Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43:14-15. 2. Bryan, F. L., and T. W. McKinley. 1974. Prevention of foodborne illness by time-temperature control of thawing, cooking, chilling and reheating turkeys in school lunch kitchens. J. Milk and Food Technol. 37:42-429. 3. Bryan, F. L., C. A. Bartleson, and N. Christopherson. 1981. Hazard analysis, in reference to Bacl1lus cereus, of boiled and fried rice in Cantonese-style restaurants. J. Food Prot. 44:5-512. 4. Gilbert, R. J. 1979. Bacillus cereus gastroenteritis. In H. Riemann and F. L. Bryan (eds.) Foodborne infections and intoxications, 2nd ed. Academic Press, New York. 5. International Commission on Microbiological Specifications for Foods. 198. Microbiological ecology of foods. vol. 1. Factors affecting life and death of microorganisms. Academic Press, New York. 6. Stiles, M. E., and L. K. Ng. 1977. The fate of enterotoxigenic bacteria inoculated into Chinese barbecued food. Can. J. Public Health 68:389-394. 7. Tiwari, N. P., V. W. Kadis, and G. C. Kemp. 1976. Comparison of the microbiological quality of Chinese and non-chinese barbecued meat obtained from Edmonton retail outlets. Can. J. Public Health 67:485-488. 8. U.S. Department of Health, Education, and Welfare, Food and Drug Administration. 1976. Food service sanitation manual. Government Printing Office, Washington, DC. Finne et al., con't.fromp. 444 14. Neal, C. W. 1977. The effects of chlorine, washing and evisceration on the microbiological population and storage life of fresh fish. M.S. Thesis. Texas A&M University, College Station, TX. 15. Newton, K. G., J. C. L. Harrison, and K. M. Smith. 1977. The effect of storage in various gaseous atmospheres on the microflora of lamb chops held at -1 C. J. Appl. Bacterial. 43:53-59. 16. Nickelson, R. 1973. Quality control- A solution to fish inspection. Proc. GnlfCaribb. lnst. 25:1-18. 17. Sander, E. H., and H. M. Soo. 1978. Increasing shelf life by carbon dioxide treatment and low temperature storage of bulk pack fresh chickens packaged in nylon/surlyn film. J. Food Sci. 43:1519-1527. 18. Silliker, I. H., R. E. Woodruff, J. R. Lugg, S. K. Wolfe, and W. D. Brown. 1977. Preservation of refrigerated meats with controlled atmospheres: treatment and post-treatment effects of carbon dioxide on pork and beef. Meat Sci.1:195-24. 19. Stansby, M. E. 1963. Analytical methods. p. 367-373. In M. E. Stansby (ed.) Industrial fishery technology. Robert E. Krieger Publ. Co.. Huntington, NY. 2. Stansby. M. E., and F. P. Griffiths. 1935. Carbon dioxide in handling fresh fish. (Haddock). Ind. Eng. Chern. 27:1452-1458. 21. Sutherland, J.P., P. A. Gibbs, J. T. Patterson, and J. G. Murray. 1976. Biochemical changes in vacuum-packaged beef occurring during storage at -2C. J. Food Technol. 11:171-18. 22. Sutherland, J.P., J. T. Patterson, P. A. Gibbs, and J. G. Murray. 1975. Some metabolic and biochemical characteristics of representative microbial isolates from vacuum-packaged beef. 1. Appl. Bacterial. 39:239-249. 23. Sutherland, J.P., J. T. Patterson, P. A. Gibbs, and J. G. Murray. 1977. The effect of several gaseous atmospheres on the multiplication of organisms isolated from vacuum-packaged beef. J. Food Technol.l2:249-255. 24. Taylor, A. A., and D. B. McDougall. 1973. Fresh beef packed in mixtures of oxygen and carbon dioxide. J. Food Technol. 8:453-461. 25. Vanderzant, C., B. F. Cobb, III, and C. A. Thompson, Jr. 1973. Microbial flora, chemical characteristics and shelf life of four species of pond-reared shrimp. J. Milk Food Technol. 36:443-446. 26. Vanderzant, C., and R. Nickelson. 1969. A microbiological examination of muscle tissue of beef, pork and lamb carcasses. J. Milk Food Technol. 32:357-361. 27. Veranth, M. F., and K. Robe. 1979. COrenriched atmosphere keeps fish fresh more than twice as long. Food Process. 4:76-79. 28. Windsor, M. L., and T. Thoma. 1974. Chemical preservation of industrial fish. New preservative mixtures. J. Sci. Food Agric. 25:993-15. 29. Wolfe, S. K. 198. Use of CO- and C 2 -enriched atmospheres for meats, fish and produce. Food Techno!. 34:55-63. 3. Yeh, C. P., R. Nickelson, II, and G. Finne. 1978. Ammoniaproducing enzymes in white shrimp tails. J. Food Sci. 43:14-142. 31. Yokoseki, M., H. Uchiyama, and I. Amano. 1956. Studies on the preservation of fish cakes. IV. Factors involved in preservative effect of carbon dioxide. Bull. Jpn. Soc. Sci. Fish. 22:35-4. JOURNAL OF FOOD PROTECTION. VOL.45,APRIL 1982