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Enterobacteriaceae and Related Organisms Isolated from Shell Eggs Collected During Commercial Processing

M. T. Musgrove^*,1, J. K. Northcutt^*, D. R. Jones^*, N. A. Cox^* and M. A. Harrison

^* Agricultural Research Service, USDA, Richard B. Russell Agricultural Research Center, Athens, GA 30605; and Department of Food Science and Technology, University of Georgia, Athens 30602

¹ Corresponding author: Mike.musgrove{at}ars.usda.gov

	ABSTRACT

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In the United States, commercial shell eggs are washed and graded before retail. Since passage of the Egg Products Inspection Act in 1971, processing guidelines have been set to ensure that external and internal characteristics are maintained. However, less is known about how commercial processing affects the safety of shell eggs. To identify enteric bacteria entering plants and persisting throughout processing, eggs were collected from 3 US commercial shell egg-processing plants on 3 separate visits. On each plant visit, 12 eggs were collected from each of 12 sites along the processing line: accumulator, prewash rinse, first washer, second washer, sanitizer rinse, dryer, oiler, check detection/scales, 2 egg grader/packer head lanes, rewash belt entrance, and rewash belt exit. Each egg was sampled by a rinse technique, and the rinsate was plated onto violet red bile glucose agar with overlay for the detection and enumeration of Enterobacteriaceae. From each plate, up to 5 colonies were randomly selected and isolated for identification to genus or species by using biochemical tests. Several genera and species were detected at each of the 3 plants. Sites from which the greatest numbers of isolates were identified were those collected from eggs during preprocessing (accumulator, prewash rinse) or from eggs judged as dirty (rewash belt entrance or exit). Sites yielding the smallest number of isolates were those during or at the end of processing. Escherichia coli and Enterobacter spp. were isolated from each of the 9 plant visits. Other genera isolated from at least 1 of the 3 plants included Cedecea, Citrobacter, Erwinia, Hafnia, Klebsiella, Kluyvera, Leclercia, Morganella, Proteus, Providencia, Rahnella, Salmonella, and Serratia. Non-Enterobacteriaceae isolated and identified included Aeromonas, Chryseomonas, Listonella, Pseudomonas, Sphingobacterium, Vibrio, and Xanthomonas. All of the genera and species were recovered less frequently from fully processed eggs than from unwashed eggs, indicating that shell eggs are less contaminated with bacteria as a result of commercial washing procedures.

Key Words: shell egg • Enterobacteriaceae • commercial processing

	INTRODUCTION

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In the United States, Canada, and Japan, shell eggs are washed and graded before being packaged for retail (Zeidler, 2002). Although washing eggs was once disallowed in the United States, it is now required for all retail shell eggs (Food and Drug Administration, 2000; USDA, 2004). Washing eggs with water colder than the egg, with water heavily contaminated with bacteria, with water containing large amounts of soluble iron, or in machines whose surfaces are contaminated with large numbers of microorganisms are factors determined to increase the chances of bacterial cross-contamination during egg washing (Moats, 1978; Baker and Bruce, 1994; Zeidler, 2002; Hutchison et al., 2003). Such conditions are addressed in Agricultural Marketing Service guidelines (USDA, 2004). Appropriate detergents, sanitizers, sanitizer levels, and defoamers; prompt drying of washed eggs; changing of the wash water at least every 4 h; and prohibition of soaking are other washing conditions addressed by the guidelines. When attention is given to these conditions, modern commercial shell egg-washing operations result in improved microbiological egg quality (Moats, 1978; Baker and Bruce, 1994; Musgrove et al., 2005a,b). This program guarantees consumers that shell eggs produced by Agricultural Marketing Service graded facilities will meet quality and size standards and are under continuous inspection (USDA, 2004).

Currently, the Food Safety Inspection Service, the USDA regulatory agency for meat and poultry, is drafting safety-based policies (Hazard Analysis and Critical Control Point systems) for the shell egg industry (Carson, 2000). Development of Hazard Analysis and Critical Control Point plans requires scientific data to be effective and practical (USDA, 1996). Over the years, many microbiological surveys have been conducted in commercial shell egg facilities (Haines, 1938; Florian and Trussell, 1956; Board et al., 1964; Moats, 1980; Davies and Breslin, 2003). However, few of them have been designed to address specific aspects of modern shell egg processes. Previously published papers describe in greater detail how processing affects bacterial population numbers and the prevalence of aerobic microorganisms, Enterobacteriaceae, Escherichia coli, and Salmonella spp. (Musgrove et al. 2005a,b). Another previously published report describes antimicrobial resistance patterns for Salmonella spp. and E. coli isolated from the same eggs (Musgrove et al. 2006). Our goal for this study was to determine the number of Enterobacteriaceae and related species associated with shell eggs as they progressed through the processing chain. This study was undertaken to characterize not only Enterobacteriaceae and related species with washed and unwashed eggs, but also those microorganisms that persisted during operations in 3 commercial shell egg-washing facilities in the Southeastern United States.

	MATERIALS AND METHODS

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Sample Collection

This study is a companion to a previously reported study (Musgrove et al., 2005a). Data collected in the previous study augment the understanding of data reported here. A survey was conducted of inline egg-processing facilities. Three commercial plants were selected for sampling on 3 separate processing days (9 visits during the entire study). These plants were designated as X, Y, and Z to protect the anonymity of the participating companies. Eggs were collected at the following points of processing: the accumulator, prewash wetting, after the first washer, the second washer, sanitizing, drying, oiling, check detection and weighing, packaging (2 different packer head belts), entrance of the rewash belt, and exit of the rewash belt. Eggs were collected after the line had been operating for at least 2 h but during the midmorning break so as not to interfere with processing. This also allowed samples to be taken simultaneously from all sampling sites. Twelve eggs from each collection site were aseptically placed into clean foam cartons, packed into half-cases, and transported back to the laboratory. Participating plants were chosen based not only on their operational procedures and willingness to participate but also on their proximity to our research facility so that eggs could be collected and analyzed expeditiously.

Sample Preparation

Upon reaching the laboratory, each egg was aseptically transferred to a sterile Ziploc bag and 10 mL of warm PBS was added. A rinse sample was obtained by shaking the bag by hand for 1 min. Rinsates were stored overnight at 4°C until microbiological analyses were performed.

Cultural Techniques

Enterobacteriaceae were enumerated by duplicate plating of 1-mL aliquots of egg rinsate onto violet red bile glucose agar as reported in a previous work (Musgrove et al., 2005a). As many as 5 isolates for each positive sample were randomly selected from presumptive Enterobacteriaceae (dark red to purple colonies with red-purple haloes). These randomly selected isolates were subjected to further analyses. A numbered circular grid (10 cm in diameter with 1-cm² divisions) and random number tables (Steel and Torrie, 1980) were used to select isolates from plates with greater than 20 colonies. Each selected isolate was streaked for purity onto plate count agar plates and incubated at 37°C overnight. The procedure was repeated twice with an isolated colony to ensure purity. An isolate from the third streak plate was saved on brain heart infusion agar slants incubated at 37°C and Protect beads (Technical Service Consultants Ltd., Heywood, Lancashire, UK). Slants and beads were then stored at 4 and –20°C, respectively, until identification analyses were performed.

Identification of Isolates

Each stored isolate was streaked onto plate count agar plates and incubated overnight at 37°C. A cultural suspension with 5 mL of physiological saline was prepared from each isolate. This material was used to inoculate bioMérieux API 20 E strips (bioMérieux, Marcy-l’Etoile, France). Strips were inoculated, incubated, handled, and analyzed according to the manufacturer’s instructions. Reactions were recorded and identifications were determined by using APILab Plus software (bioMérieux).

Statistical Analysis

The number of times a genus was identified from isolates recovered from eggshells collected before, during, or after processing was divided by the possible number of times it could have been recovered and identified (0/9 to 9/9). These ratios were analyzed by using the ² test for equal proportions [P < 0.05 (all genera except for Salmonella); P < 0.10 (Salmonella); SAS Institute, 1999]. The number of isolates recovered from eggshells collected at distinct stages of the process (before, during, or after processing) at plants X, Y, and Z were divided by the total number of isolates recovered for that plant. These ratios were analyzed by using the ² test for equal proportions (P < 0.05). Additionally, ratios for each of the distinct processing stages were analyzed from plant to plant by using the same procedure.

	RESULTS

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Identified isolates were grouped by plant (X, Y, Z), combining data for all 3 plant visits. For each plant, identified isolates were tabulated alphabetically and arranged into Tables 1 to 3. In each of these tables, the number of isolates for a given species is listed for each of the 12 sample sites from which the egg was collected. There are 30 genera in the bacterial family Enterobacteriaceae (Holt et al., 2000b), and half of them were recovered at least once from eggs collected at the 3 shell egg-processing plants. Escherichia coli was the most frequently isolated bacterial species, recovered from the shells of eggs collected from all 12 of the sites along the processing chain.

	DISCUSSION

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Random selection of colonies from violet red bile glucose agar plates allowed for the determination of prevalent species on eggshells at the stage of processing during which they were collected. A total of 837 isolates were identified. During the 9 visits (3 per plant), 549 isolates were identified from plant X, 68 were identified from plant Y, and 220 were identified from plant Z. Plant X was the oldest of the 3 plants. Plant Y was the only facility that did not rewash eggs visually determined to be too dirty or stained for USDA Grade A eggs (USDA, 2000). It is possible that by diverting dirty eggs to a breaker plant and not rewashing them, less cross-contamination occurred in the washers at plant Y. Plant Z was the only facility that did not oil eggs.

Table 5 contains information on the percentage of Enterobacteriaceae found at each stage of processing. For all 3 plants, significant percentages (P < 0.05) of the identified isolates were from shell rinses of eggs collected during preprocessing (accumulator, prewash rinse, rewash entrance, rewash exit). Eggs from these 4 sites (before) accounted for 70.3% (386/549), 77.9% (53/68), and 83.2% (183/220) of identified isolates for plants X, Y, and Z, respectively. Significantly higher proportions (P < 0.05) of isolates were identified from eggs collected from in-process (during) sample sites (washer 1, washer 2, sanitizer rinse, dryer, oiler) for plant X (24.6%; 135/549) than for plant Y (10.3%; 7/68) or plant Z (10.0%; 22/220). A related report contains more information on the population dynamics at each facility (Musgrove et al., 2005a). Wash water conditions were described in greater detail in another report (Northcutt et al., 2005). Plant X had lower wash water pH and temperature measurements than the other 2 plants (Musgrove et al., 2005a). However, only 5.1% (28/549), 11.8% (8/68), and 6.8% (15/220) of the total isolates from each of the respective plants persisted through the processing chain (after). For every facility, significantly more organisms (P < 0.05) were removed by the commercial washing process for shell eggs than remained on them when compared with the number of isolates identified from eggs collected before processing began.

Most of the identified isolates from all 3 plants were members of the family Enterobacteriaceae, although other related organisms were recovered. Chryseomonas, Pseudomonas, Sphingobacterium, and Xanthomonas, Group 4 gram-negative aerobic-microaerophilic rods and cocci (Holt et al., 2000a), were occasionally isolated from plants X and Y. These organisms accounted for only 1.4% of all those identified. Chryseomonas luteola, Pseudomonas spp., Pseudomonas aeruginosa, Pseudomonas cepacia, Sphingobacterium multivorum, and Xanthomonas maltophilia were recovered from plant X samples (X1 and X2), whereas P. cepacia was the only group 4 species isolated from plant Y samples (Y3). In both the first and second visit to plant X, wash water pH values were 9.9 and 9.1, respectively (Musgrove et al., 2005a). A wash water sample pH of 10 was recorded for the first and third visit to plant Y (Y1 and Y3), although the temperature was lower for the latter (44.3°C compared with 43.9°C). Washer water pH values were greater than 11 for each of the 3 visits to plant Z. Kinner and Moats (1981) reported that bacterial counts increased at pH 7 and 8 in simulated wash water at 35, 40, and 45°C. Counts decreased very slowly at pH 9 and 45°C, whereas at pH 10 or 11, counts decreased regardless of temperature. However, this was a laboratory experiment involving synthesized wash water, not actual wash water over an 8-h time period. Excessive foaming, increased solids, and a concomitant rise in chemical oxygen debt caused by eggs breaking during the washing process may have contributed to the ability of these species to survive under field conditions. In fact, Kinner and Moats (1981) showed that adding 1% suspended whole egg solids increased survivability of Pseudomonas, Flavobacterium, and Citrobacter. Nonetheless, Chryseomonas, Pseudomonas, Sphingobacterium, and Xanthomonas were not recovered from the shells of eggs that had completed the processing chain in any of the plants that participated in our study. Agricultural Marketing Service guidelines, as described in the Code of Federal Regulations 7 Part 56 (USDA, 2004), were designed in part to improve shell egg quality, which includes decreasing the incidence of spoilage organisms on processed and packaged products. These genera have either been associated with spoilage or are basonyms of genera associated with spoilage (Board et al., 1964; Baker and Bruce, 1994).

Vibrionaceae is the second subgroup or family in group 5 (facultative anaerobic gram-negative rods; Holt et al., 2000b). These organisms are found worldwide and often occur aquatically. Several species are pathogenic for humans, fish, and amphibians. Some species of Vibrio and Aeromonas can cause diarrhea, septicemia, or infect wounds. Once considered Vibrionaceae, aeromonads have been transferred to the family Aeromonadaceae (Isonhood and Drake, 2002). Members of both of these closely related families were recovered from 7 of the 9 plant visits and accounted for 4.6% of total isolates identified. Aeromonas spp. were recovered from plant X on 3 visits and from plant Z on the first and third visits (Z1 and Z3). These organisms are ubiquitous in many foods and may play a role in foodborne disease (Isonhood and Drake, 2002). Aeromonas spp. are psychrotrophic organisms, and their presence is of concern in refrigerator-stored foods such as eggs (Daskalov, 2006). Listonella damsela, once classified as Vibrio damsela, was first proposed as a genus in 1985 (MacDonnell and Colwell, 1985). Its human clinical significance is limited to necrotizing wounds following sea water exposure. This species was identified from eggshell rinses from all 3 plants. Vibrio spp., including Vibrio metschnikovii, were recovered only at plant Z during the first and third visits, respectively. Some species of Vibrio have been implicated in wound infections and diarrheal foodborne disease (Holt et al., 2000b). Aeromonads survived processing in plant X (X3, 1/12) and plant Z (Z3, 7/10) eggs, whereas a single isolate of L. damsela survived processing in a plant X (X2) egg. An isolate of V. metschnikovii survived on a Z3 egg. As described in Table 4, Aeromonas and Vibrio persisted through processing in 2/9 and 1/9 visits even though they were present in only 5/9 and 2/9 visits before washing. Most of the other organisms that persisted through processing were those collected from unwashed eggs in 8 or 9 of the 9 visits (e.g., E. coli, Enterobacter, or Klebsiella). Other factors that may have contributed to the survival of Aeromonas, Listonella, and Vibrio are the physiological and physical adaptations caused by their aquatic nature, which contributed to their withstanding water-based intervention steps (Holt et al. 2000b; Isonhood and Drake, 2002). Aeromonas enrichment methodology includes alkaline broths, an indication that these organisms are favored by such conditions (Millership and Chattopadhyay, 1984). Average pH values for wash water, as reported in previously published work, ranged from 9.1 to 11.3 (Northcutt et al., 2005).

Other researchers have reported on genera and species associated with shell eggs (Haines, 1938; Florian and Trussell, 1956; Board et al., 1964, 1966; Moats, 1980). Bacteria from 16 genera were recovered from eggshells in one survey of gram-positive and gram-negative species. Pseudomonas, Flavobacterium, Escherichia, Aerobacter, Aeromonas, Proteus, and Serratia are organisms mentioned in that survey that were also recovered in the current study (Board et al., 1964). Flavobacterium and Aerobacter are the basonyms of Sphingobacterium and Enterobacter. In a 1938 study, Haines reported that 38% of eggshell microorganisms are gram negative. Moats (1980) reported that 39% of the isolates from unwashed shell eggs were gram negative. Pseudomonas, Escherichia, Aerobacter, and Aeromonas were isolated from eggs graded as A, B, and C quality. Flavobacterium and Escherichia were found on shells of washed and unwashed eggs, although the latter were enumerated far more often. Board et al. (1964) reported that Escherichia, Aerobacter, and Pseudomonas were isolated from clean, lightly soiled, and cracked eggs, whereas Aeromonas were recovered from clean and cracked eggs. A majority of the isolates that were identified in the current study were recovered from shell rinses of eggs collected at one of the preprocessing sampling sites: accumulator, prewash rinse, rewash entrance, and rewash exit.

In another study recently conducted in our laboratory, Enterobacteriaceae were recovered from washed and unwashed shell eggs during 6 wk of storage (Jones et al., 2004). In that study, 105 isolates were identified, most of them from unwashed eggs (Musgrove et al., 2004). Genera identified in the previously published work but not recovered in our present study include Pantoea and Yersinia. There were many more isolates in the present study and more genera were detected that were absent from the previous study: Aeromonas, Cedecea, Chryseomonas, Erwinia, Hafnia, Leclercia, Listonella, Morganella, Proteus, Sphingobacterium, and Vibrio (Musgrove et al., 2004). However, the current study involved 10 times the number of eggs and isolates and 2 more plants than were included in the previous study.

Escherichia coli and Enterobacter spp. were isolated from every plant and during every visit in the current study and accounted for 55.8% (467/837) of isolates identified. Escherichia fergusonii and Escherichia vulneris were also isolated, but never from fully processed eggs. Escherichia coli was isolated more often than any other single species. Escherichia coli constituted 25.9% (142/549), 45.6% (31/68), and 26.8% (59/220) of the isolates identified from any sample site at plants X, Y, and Z, respectively. However, only 2.1% (3/142), 12.9% (4/31), and 8.5% (5/59) of them remained on eggshells collected at the end of the processing chain. Mountney and Day (1970) suggest that, in some cases, E. coli may adapt and survive quaternary ammonium detergents, although few of them seem to have survived in our study. Enterobacter spp. accounted for 24.6% (135/549), 25% (17/68), and 32.7% (72/220) of the isolates identified in plants X, Y, and Z, respectively. Of these isolates, only 5.9% (8/135), 5.9% (1/17), and 0% (0/72) survived processing at each of the plants.

Enterobacter sakazakii, a species that may contaminate soy-based infant formulas (Muytjens et al., 1988), was also isolated from eggshells collected at every processing plant in our study. However, this organism was never isolated from fully processed eggs. Recently, E. sakazakii has appeared in fly larvae, in food-processing plants, and in the home environment (Hamilton et al., 2003; Kandhai et al., 2004). Salmonella was presumptively identified in each of the 3 plants in our study. A large number of the presumptive Salmonella were identified from pre- or in-process isolates during the first visit to plant X (X1). One of the 3 tap water samples collected during that replication was also found to be Salmonella positive. Additionally, the lowest wash water pH and temperatures for any of the plant visits was recorded for the X1 visit. In addition, excessive foaming was noted in both washers (Musgrove et al., 2005a). These data underscore the need for maintaining optimal water conditions when washing eggs.

A few of the organisms isolated and presumptively identified in this study are considered to be foodborne pathogens (Salmonella, E. sakazakii, Vibrio spp., and Aeromonas hydrophila). Others may be opportunistic or rare human pathogens (Holt et al., 2000a,b). A number of the isolates recovered in this study were similar to those recovered in previously published reports. However, this study has provided a comprehensive look at Enterobacteriaceae and related organisms as they persist or are eliminated during commercial operations in 3 US commercial shell egg plants. Perfecting the effectiveness of the process should always be a goal; however, these data indicate that commercial washing procedures are successful in removing a significant proportion of the Enterobacteriaceae types and related organisms from shell eggs.

	ACKNOWLEDGMENTS

 
The authors gratefully acknowledge the expert technical assistance of Jordan Shaw, Patsy Mason, Sherry Turner, and Manju Amin. This work was funded in part by a grant from the United States Poultry & Egg Association (Atlanta, GA) (RE project number 501), and their support is greatly appreciated.

Received for publication December 6, 2007. Accepted for publication December 27, 2007.

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