ENVIRONMENT AND HEALTH Incidence of Salmonella in Fresh Dressed Turkeys Raised Under Salmonella-Controlled and Uncontrolled Environments DOUGLAS F. CAMPBELL,1 STANLEY S. GREEN, 2 CARL S. CUSTER1'3 and RALPH W. JOHNSTON 2 US Department of Agriculture, Food Safety and Inspection Service, Beltsville, Maryland 20705, and Washington, DC 20250 (Received for publication October 13, 1981)
1982 Poultry Science 61:1962-1967 INTRODUCTION
In-plant samples of turkeys raised in a salmonella-controlled environment were collected at three turkey processing plants in Minnesota in the fall of 1979. The birds were raised by commercial growers who cooperated closely with researchers from the Department of Veterinary Pathobiology at the University of Minnesota working under a grant from the US Department of Agriculture (USDA), Animal Plant Health Inspection Service, Division of Veterinary Services. The growing turkeys were closely monitored for the presence of salmonella by analyzing environmental samples of dust and litter, feed samples, cloacal swabs, blood samples, and hatchery debris. Salmonella-controlled flocks (experimental) were monitored over several months and <.05% of the samples were positive for salmonella (Veterinary Services, unpublished data). Data indicated that upon leaving the growing farm for slaughter, die experimental turkey flocks, if not salmonella-free, had an extremely low incidence of salmonella.
building 322, BARC-East, Beltsville, MD 20705. 2 Agriculture Annex, 12th and C Streets, S. W., Washington, DC 20250. 'Present address: US Department of Agriculture, Food Safety and Inspection Service, Processed Products Inspection Division, South Building, Room 2159, 12th and Independence Avenue, S. W., Washington, DC 20250.
The purpose of this study was to determine the salmonella level in eviscerated turkeys derived from these specially reared flocks compared to turkeys from conventionally reared flocks ("normal" flocks). This permits a judgment on the degree of contamination that occurs during the slaughter and evisceration process. MATERIALS AND METHODS Sampling Sampling was conducted on two consecutive days in each of three different turkey slaughtering plants in Minnesota. One day was for sampling the normal turkeys; the other day was for sampling the experimental turkeys. The three plants were owned by the same company. Two commercial growers supplied the experimental turkeys and the normal birds were purchased from several suppliers. Samples of the scald and chiller waters, swabs of the product contact surfaces of various pickers, tables, belts, and chutes, and whole bird rinsings were collected. The rinse method was chosen because it has been shown to be an excellent method for salmonella recovery in poultry (Cox et al., 1978). The water samples were collected at the overflow pipes of the scald and chill tanks by filling labeled, sterile diluent bottles containing 10 ml of 10 X lactose broth with 90 ml of the respective water samples. Swab samples were
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ABSTRACT The incidence of salmonella in turkeys from experimental salmonella-controlled and uncontrolled, or normal, flocks processed at three turkey slaughter plants were compared. The results indicate that processing salmonella-controlled turkeys in a plant that routinely kills normal birds may result in the contamination of the salmonella-controlled birds, probably due to salmonella in the plant environment. The salmonella-controlled turkeys studied tended to have a lower incidence of salmonella than normal birds. These observation indicate that salmonella control practices in turkey raising can result in a salmonella reduction in market birds even under existing commercial slaughter, evisceration, and cooling procedures. (Key words: salmonella, turkeys, commercial slaughter, evisceration, chilling, processing)
SALMONELLA IN FRESH DRESSED TURKEYS
filled, closed funnel. The corner was dipped in a chlorine solution of about 1,000 ppm, and rinsed with potable water. The filled corner was raised, the end removed aseptically, and by using the bag as a funnel, the rinsing was drained into a properly labeled container containing sodium thiosulfate (.2 mg/ml) to neutralize any residual chlorine. All samples were frozen promptly and shipped by air freight under dry ice to the Beltsville laboratory. A total of 259 whole bird rinsings, 49 swabs, and 31 water samples were collected. Laboratory
Methods
Each gauze swab was removed from its bag, placed in 100 ml of sterile lactose broth containing .6% tergitol, shaken 25 times, and incubated 24 hr at 35 C as the lactose preenrichment. Further methods for isolation and identification of salmonella have been described (USDA, 1974). The containers of water samples were thawed rapidly in a tub of circulating cold tap water, .6% tergitol was added, and the pH was
TABLE 1. Swab samples of equipment in plants slaughtering experimental salmonella-cotrolled and normal turkey flocks Salmonella (no. positive/no. samples) Sampling site
Plant
Experimental Serotypes
Normal Serotype
A B C
0/4 0/6
0/4 0/6
2/6 S. hadar, S. st. paul
3/6 S. hadar, S. beidelberg
Pickers before startup
Chutes at chiller entry before startup A
0/1 0/1
B C
0/1 0/1
A B
0/1
0/2
C
1/1 S. litchfield
0/1
A B C
0/1 0/1 0/1
0/1 0/1 0/1
B
1/1 S. derby
Chutes at chiller entry end of sampling
Chutes at chiller exit before startup
Frame of opening between
scaled and evisceration rooms, before startup Chute at chiller exit end of sampling
0/1
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collected by swabbing large areas of product contact surfaces, including individual pickers, conveyor belts, chutes, and tables with sterile 3 X 3 in (7.62 X 7.62 cm) gauze pads, then placing each pad in an appropriately labeled sterile Whirl-Pak bag. The pickers were swabbed only before start-up and the other equipment was swabbed before start-up and at the end of the sampling period, when possible. Swabs were analyzed for the presence or absence of salmonella. Whole turkey rinsings were obtained nondestructively. The carcasses were aseptically caught in heavy duty 30 gal plastic trash bags as they exited the chiller. After adding 600 ml of the rinse fluid into the body cavity, the bag was closed, and by firmly gripping the carcass, the bag was vigorously shaken 30 times, rotating the bag and contents one-third turn every 10 shakes. The rinse solution was aseptically collected after the carcass was aseptically drained, removed from the bag, and returned to the processing line. To collect the rinsing, the top and one bottom corner of the bag were held which caused the other corner to act as a
1963
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CAMPBELL ET AL.
whole bird rinsings had to be done using tap water with a crystal of sodium thiosulfate to neutralize residual chlorine. These samples were frozen and transported to the laboratory and thawed in cold tap water. Then, to the water rinsing, sufficient lactose at 10 X normal strength was added, resulting in a single strength lactose solution. From this point, the samples were treated exactly as the whole bird lactose rinsings. RESULTS Table 1 presents the results of the swab samples of the equipment. All the swabs in plant A were salmonella negative. In plant B, the only positive swab was from the frame of an opening where the shackle line conveyed the birds from the scald room to the evisceration area. Visual inspection revealed that this opening had been neglected during the cleanup of the prevous day. The presence of Salmonella derby indicated that the contamination was from the normal flock of the previous day, which had S. derby isolated from the bird rinse samples. Swabs from plant C revealed salmonella on the pickers and the chiller entry chute, before start-up, indicating an inadequate cleanup. The presence of salmonella on equipment, particularly before start-up, can act as a source of contamination for turkeys during processing (Bryan et al., 1968; Dawson et al, 1979; Hacking et al, 1968; Nivas et al, 1973; Patterson, 1971; Schuler and Badenhop,1972). Table 2 shows the distribution of salmonella isolates on the turkeys at the chiller exit. Salmonella hadar was isolated from three flocks in two different plants, and in the chiller water of the third plant (Table 3). To the best of the authors' knowledge, this
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adjusted to 7.0. Portions equivalent to 75 ml, 10 ml, and 1 ml were incubated 24 hr at 35 C as the lactose preenrichment. Further methods for isolation and identification of salmonella have been described (USDA, 1974). The whole bird lactose rinsings were thawed rapidly in a tub of circulating cold tap water. Then 281 ml of the thawed sample were placed into a sterile container and an equal volume of double strength tetrathionate broth was added and mixed. Portions equivalent to 270 ml, 10 ml, and 1 ml of the original broth rinsing were made and incubated 24 hr at 35 C. Further methods for isolation and identification of salmonella have been described (USDA, 1974). Due to unforseen circumstances, some of the
SALMONELLA IN FRESH DRESSED TURKEYS
through the tank that day. Although plants A and B had much lower incidences of salmonella in the experimental flocks than in the normal flocks, plant C had a higher contamination rate in the experimental flock. The overall incidence rate of salmonella in the experimental carcasses was lower than in the normal carcasses but was not statistically significant (Table 4). DISCUSSION After crating and loading on the transport trucks, the experimental turkeys were treated exactly as normal birds during shipment and processing at the plant. In a plant that routinely kills normally raised turkeys, processing an occasional flock of experimental turkeys presents a problem, such as having these birds remain salmonella free through the evisceration process. Salmonella are common in the live bird areas (Dawson et al., 1979; Zottola et al, 1970), and there are high levels of airborne bacteria in the scald area as well (Patterson, 1973). The separation of the live bird and scald areas can help reduce airborne bacterial levels and lessen the chances for contamination throughout the plant. It has been reported that salmonella-infected flocks can be identified before slaughter and scheduled for slaughter at the end of the day to reduce the chances of cross contamination (McBride et al., 1978). Conversely, flocks known to have little or no salmonella, as the experiemental flocks, could be killed early in
TABLE 3. Levels of salmonella in scald and chill tank water samples collected in plants slaughtering experimental salmonella-controlled and normal turkey flocks
Sample site
Plant
Scald tank before startup
A B C A B C A B C A B C
Scald tank end of sampling
Chill tank before startup
Chill tank end of sampling
Salmonella (no. positive/no. samples) Normal Serotype Experimental 0/1 0/1 0/1
0/1 0/1 0/1
0/1 0/1 0/1
0/2 0/1 0/1
0/1 0/1 0/2
0/1 0/1 0/2
0/2 0/1 0/2
1/2 1/2 S. hadar pos. in 75 ml. 1/1 1/1 S. hadar pos. in 10 ml. 0/2
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was the first time this uncommon serotype S. hadar had been isolated in market turkey carcasses in the United States. It may be that S. hadar is becoming established in the United States, as it is in Britain and Canada (Center for Disease Control, 1980; Rowe et al, 1980). The high incidence of only S. litchfield in the experimental turkeys processed in plant C indicates that this flock was contaminated with S. litchfield before it entered the plant. Contamination during shipping has been suggested previously by Rigby et al. (1980). Salmonella litchfield was not recovered from any other samples in plant C, including the normal flock of the previous day, or from the pre-operational samples taken on the day the experimental flock was killed. The large volume sample (270 ml) was used because a sample size of 10 ml could have reduced the potential number of salmonella recoveries, due to low levels of salmonella, as has been reported in chickens by Surkiewicz et al, 1969. The results justified the need for the large rinse sample. Table 3 presents the results of the water samples collected from the scald and chill tanks at the three plants. The scald tanks in each plant were a constant 61 C, and no significant fluctuation was noted during production. Salmonella were isolated from the chill tanks of plant A and B at the end of the sampling period, but no other samples were positive. The presence of S. hadar in both the 75 and 10 ml portions of the chill tank samples indicates that a flock contaminated with S. hadar had passed
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CAMPBELL ET AL.
the day in an effort to minimize salmonella contamination. Although there was a statistically significant difference in the incidence of salmonella between flocks in plant A, this was not the case for plants B and C, so that the total result was not statistically significant. This is primarily due to the incidence rate in the flock in plant C. However, when turkeys enter a slaughter plant free from salmonella, it is likely that the finished eviscerated birds will have a lower incidence of salmonella than normally raised turkeys.
ACKNOWLEDGMENT
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The authors gratefully acknowledge the cooperation of Satish Nivas and Ben Pomeroy of the University of Minnesota and Irvin Peterson of the USDA, APHIS, Veterinary Services. Also we thank Cynthia Szymanski, Dennis McClain, and the late Joseph Macaluso for their technical assistance.
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REFERENCES
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Bryan, F. S., J. C. Ayres, and A. A. Kraft, 1968. Contributary sources of salmonellae on turkey products. Am. J. Epidemiol. 8 7 : 5 7 8 - 5 9 1 . Center for Disease Control, 1980. Salmonella hadar —
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England and Wales — Morbidity and Mortality
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Weekly Report. October 24:504. Cox, N. A., A. J. Mercuri, D. A. Tanner, M. O. Carson,
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In this study, the serotype most often isolated from the carcass rinsings was S. hadar followed by S. litchfield. However, S. hadar and S. heidelberg were isolated from three different flocks, and no other serotype was isolated from more than one flock. There was a total absence of S. typhimurium during this study even though this serotype has been reported as the most common isolate in market turkeys (Sadler and Corstvet, 1965). This was likely due to the effort in the state of Minnesota to control S. typhimurium in turkeys. Data from this study indicate that after evisceration, although there is not a statistically significant decrease in the incidence of salmonella in carcasses processed from turkeys raised free of salmonella, there is still a reduced incidence of salmonella in such birds. The authors feel that these data indicate that efforts to reduce the salmonella carrier rate on the farm can also result in reduced salmonella in market birds, even under existing commercial processing methods. Further studies and sampling are desirable.
SALMONELLA IN FRESH DRESSED TURKEYS
Rigby, C. E., J. R. Pettit, M. F. Baker, A. H. Bentley, M. O. Salomons, and H. Lior, 1980. Sources of salmonellae in an uninfected commercially processed broiler flock. Can. J. Comp. Med. 44:267-274. Rowe, B., M.L.M. Hall, L. R. Ward, and J.D.H. deSa, 1980. Epidemic spread of Salmonella hadar in England and Wales. Br. Med. J. 280:1065-1066. Sadler, W. W., and R. E. Corstvet, 1965. Second survey of market poultry for Salmonella infection. Appl. Microbiol. 13:348—351. Schuler, G. A., and A. F. Badenhop, 1972. Microbiology survey of equipment in selected poultry processing plants. Poultry Sci. 51:830—835. Surkiewicz, B. F., R. W. Johnston, A. B. Moran, and G. W. Krumn, 1969. A bacteriological survey of chicken eviscerating plants. Food Technol. 23:80-85. US Department of Agriculture, 1974. Microbiology laboratory guidebook. Scientific Services, FSQS, USDA, Washington, DC. Zottola, E. A., D. L. Schmeltz, and J. J. Jezeski, 1970. Isolation of salmonellae and other air-borne microorganisms in turkey processing plants. J. Milk Food Technol. 33:395-399.
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