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Applied and Environmental Microbiology, December 2001, p. 5431-5436, Vol. 67, No. 12
Department of Nutrition and Food Science, University of
Maryland, College Park, Maryland 207421
and Division of Animal and Food Microbiology, Center for
Veterinary Medicine, Food and Drug Administration, Laurel, Maryland
207082
Received 3 August 2001/Accepted 26 September 2001
A total of 825 samples of retail raw meats (chicken, turkey, pork,
and beef) were examined for the presence of Escherichia coli and Salmonella serovars, and 719 of these
samples were also tested for Campylobacter spp. The
samples were randomly obtained from 59 stores of four supermarket
chains during 107 sampling visits in the Greater Washington, D.C., area
from June 1999 to July 2000. The majority (70.7%) of chicken samples
(n = 184) were contaminated with
Campylobacter, and a large percentage of the stores
visited (91%) had Campylobacter-contaminated chickens. Approximately 14% of the 172 turkey samples yielded
Campylobacter, whereas fewer pork (1.7%) and beef
(0.5%) samples were positive for this pathogen. A total of 722 Campylobacter isolates were obtained from 159 meat
samples; 53.6% of these isolates were Campylobacter jejuni, 41.3% were Campylobacter coli, and
5.1% were other species. Of the 212 chicken samples, 82 (38.7%)
yielded E. coli, while 19.0% of the beef samples,
16.3% of the pork samples, and 11.9% of the turkey samples were
positive for E. coli. However, only 25 (3.0%) of the
retail meat samples tested were positive for Salmonella.
Significant differences in the bacterial contamination rates were
observed for the four supermarket chains. This study revealed that
retail raw meats are often contaminated with food-borne pathogens;
however, there are marked differences in the prevalence of such
pathogens in different meats. Raw retail meats are potential vehicles
for transmitting food-borne diseases, and our findings stress the need
for increased implementation of hazard analysis of critical
control point (HACCP) and consumer food safety education efforts.
Microbial food safety is an
increasing public health concern worldwide. It is estimated that each
year in the United States there are approximately 76 million food-borne
illnesses (23). While most of these illnesses are
undiagnosed and thus unreported, approximately 325,000 cases result in
hospitalization, and 5,000 cases are fatal. Nearly 2.4 million cases
are caused by Campylobacter spp., 1.4 million cases are
caused by nontyphoidal Salmonella serovars, and 270,000 cases are caused by pathogenic Escherichia coli, including
E. coli O157:H7 (23). Although these pathogens usually cause mild to moderate self-limiting gastroenteritis, invasive
diseases and complications may occur, resulting in more severe cases.
For example, Campylobacter has been identified as the
predominant cause of Guillain-Barré syndrome and reactive arthritis (3). Systemic salmonellosis infections can be
life threatening, and Shiga toxin-producing E. coli (STEC),
particularly E. coli O157:H7, can cause bloody diarrhea and
hemolytic uremic syndrome (12).
Campylobacter, Salmonella, and pathogenic
E. coli all colonize the gastrointestinal tracts of a wide
range of wild and domestic animals, especially animals raised for human
consumption (24). Food contamination with these pathogens
can occur at multiple steps along the food chain, including production,
processing, distribution, retail marketing, and handling or
preparation. Numerous epidemiological reports have implicated foods of
animal origin as the major vehicles associated with illnesses caused by
food-borne pathogens (30, 34). Contaminated raw or
undercooked poultry and red meats are particularly important in
transmitting these food-borne pathogens. Other sources of human
infections with Campylobacter, Salmonella, and
STEC include contaminated produce and contact with farm animals and
pets. Person-to-person transmission has also been described
(33).
Studies worldwide have shown that Campylobacter,
Salmonella, and E. coli are often present in
fresh meat and poultry (34). However, there is a paucity
of data concerning the prevalence of contamination with multiple
food-borne pathogens in retail meats in the United States. The
objectives of this study were to determine the prevalence of
Campylobacter, Salmonella, and E. coli
in retail raw meats obtained in the Greater Washington, D.C., area and
to investigate the association of microbial contamination with product
type, season, and supermarket chain.
Sample collection and preparation.
Meat samples
(n = 825), including chicken carcasses, turkey breasts,
beef steaks, and pork chops, were randomly collected from retail stores
of four supermarket chains in the Greater Washington, D.C., area,
including suburban Maryland. Stores of the four supermarket chains in
the area were identified by using phone books, store web sites, and
store maps. Each store was assigned an identification number in order
to form a store database. Sampling visits were made on every other
Monday for 14 months (June 1999 to July 2000). On each sampling day,
four stores were randomly chosen from the store database by using a
statistical program (SAS Institute Inc., Cary, N.C.). Eight prepackaged
raw meat products (two of each meat type) were randomly selected and
transported on ice to the laboratory. Each sample was aseptically
removed and placed in a plastic bag that contained 200 to 500 ml of
buffered peptone (Difco Laboratories, Detroit, Mich.), depending on the
sample size. The bag was shaken manually for 3 min and left on ice for 20 min. The rinse solution was used for isolation of
Campylobacter, E. coli, and
Salmonella.
Bacterial isolation.
Modifications of methods described in
the Food and Drug Administration Bacteriological Analytical
Manual were used to isolate Campylobacter,
E. coli, and Salmonella from the retail raw meat samples (11). Isolation and culturing of
Campylobacter were always conducted with the AnaeroPak
system (Mitsubish Gas Chemical Co., Inc., Osaka, Japan) under
microaerophilic conditions created by using a 10%
CO2-10% H2-80%
N2 gas mixture and Campy pack (Becton Dickinson,
Cockeysville, Md.). A 20-ml portion of a meat sample rinse solution was
mixed with the same volume of double-concentrated Bolton broth (Oxoid
Inc., Ogdensburg, N.Y.) and incubated at 42°C overnight with shaking.
The overnight enrichment broth was used to inoculate
Campylobacter onto blood-free selective agar (Oxoid) plates
using a cotton swab. After 48 h of incubation at 42°C, the
plates were examined for typical Campylobacter colonies,
which were small, gray, and droplike or small and shiny or
slimy. Presumptive Campylobacter colonies were
subcultured on blood agar plates and incubated for 48 h at 42°C.
Single colonies (3-5) on a blood agar plate were selected
for Gram staining and oxidase and catalase tests.
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.12.5431-5436.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Prevalence of Campylobacter spp.,
Escherichia coli, and Salmonella Serovars in
Retail Chicken, Turkey, Pork, and Beef from the Greater Washington,
D.C., Area
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
PCR assays.
Presumptive Campylobacter isolates
that were gram-negative, curved organisms as determined by microscopic
examination and were oxidase and catalase positive were to be confirmed
members of the genus Campylobacter by performing a PCR
assay. Primers BO4263 and BO4264 amplified a 256-bp unique fragment of
Campylobacter genomes (17). A multiplex PCR
method, based on two PCR assays described by Linton et al., were
developed to identify Campylobacter species with primers HIP
400F and HIP 1134R for Campylobacter jejuni and primers
CC18F and CC519R for Campylobacter coli (20). Multiplex PCR assays were also performed for E. coli to
identify genes encoding Shiga toxins 1 and 2 and heat-labile and
heat-stable enterotoxins (17, 25, 36). The targets, primer
sequences, and sizes of amplicons for the PCR assays are shown in Table
1.
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Data analysis. Prevalence data for the microorganisms sorted by meat type, season, and store chain were analyzed by using the analysis of variance of SAS for Windows (version 6.12; SAS Institute Inc.).
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Fifty-nine stores, including 29 chain A stores, 17 chain B stores,
9 chain C stores, and 4 chain D stores, were visited a total of 107 times from June 1999 to July 2000. Thirty of these stores were visited
once, 15 stores were visited twice, 9 stores were visited three times,
and 5 stores were visited four times. A total of 825 samples of retail
raw meats were collected and examined for the presence of E. coli and Salmonella; 719 of these samples were also
tested for the presence of Campylobacter. (Table 2).
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Prevalence of Campylobacter, E. coli, and Salmonella. Table 2 shows the prevalence of Campylobacter, E. coli, and Salmonella in retail chicken, turkey, pork, and beef obtained from the 59 stores. Of the four raw meat products, chicken was most frequently contaminated with Campylobacter (70.7%), followed by turkey (14.5%). Compared to poultry, red meats had much lower rates of contamination with Campylobacter. Less than 1% of beef samples and less than 2% of pork samples were positive for this pathogen. Chicken also had the highest rate of E. coli contamination (38.7%). Interestingly, beef (19.0%) and pork (16.3%) were more likely contaminated with E. coli than turkey was (11.9%). In contrast, Salmonella was isolated from only 3.0% of the 825 meat samples, and chicken had the highest rate of Salmonella contamination (4.2%).
A number of meat samples were contaminated either with Campylobacter and E. coli or with Campylobacter and Salmonella. Of 184 chicken samples tested, 54 (29.3%) were contaminated with both Campylobacter and E. coli, and 2 were positive for all three bacteria. Only five pork samples and four turkey samples had more than one type of organism present. The five pork samples contained E. coli and Salmonella, whereas only one turkey sample contained E. coli and Salmonella. Two turkey samples were contaminated with Campylobacter and E. coli, and one turkey sample was contaminated with Campylobacter and Salmonella. In contrast, none of the beef samples contained detectable numbers of more than one of the three enteric bacteria.Isolation of Campylobacter, E. coli, and Salmonella sorted by store and supermarket chain. Most (91%) of the stores during 92 sampling visits had Campylobacter-contaminated chicken. Only 22 (24%) of the store visits yielded Campylobacter-positive turkey samples. E. coli was recovered from chicken after nearly 60% of 106 store visits, whereas E. coli was recovered from pork, beef, and turkey after 24, 23, and 19% of the store visits, respectively. However, very few stores had Campylobacter-contaminated beef (1%) or pork (3%). Due to the low prevalence of Salmonella, no significant difference was observed among the stores that were positive for the presence of Salmonella regardless of the type of meat tested.
During the 14-month sample collection period, five stores of three supermarket chains were visited four times. Regardless of the store visited, Campylobacter was repeatedly found in one or two of the two chicken samples analyzed except for the initial visit to one store. Chicken samples were also frequently (60% of the visits) contaminated with E. coli. Salmonella, however, was isolated only from one turkey sample and one beef sample from one store after the fourth visit. The microbial contamination rates for the four supermarket chains ranged from 20.6 to 32.6% for Campylobacter, from 18.1 to 28.3% for E. coli, and from 0 to 3.4% for Salmonella (Table 3). Similar to the findings obtained when the retail meats were compared, there were not significant differences in the levels of Salmonella contamination among the four chains. However, the Campylobacter and E. coli contamination rates for the four supermarket chains were significantly different (P < 0.05). Chain D had higher microbial contamination rates for both Campylobacter and E. coli than chains A and B and a higher E. coli contamination rate than chain C.
|
PCR results for Campylobacter identification and
E. coli toxins.
A total of 722 isolates (three to
five isolates per sample) from 159 meat samples that were presumptively
Campylobacter positive (Table
4) were identified based on Gram staining
and oxidase and catalase tests. A PCR assay specific for C. jejuni, C. coli, and Campylobacter upsaliensis
confirmed that almost all of the isolates were Campylobacter
isolates; the only exceptions were three isolates from chicken and one
isolate from turkey. Approximately one-half (53.6%) of the isolates
were identified as C. jejuni, 41.3% were identified as
C. coli, and 5.1% were identified as other species. Both
C. jejuni and C. coli were isolated more
frequently from retail chicken than from turkey, pork, or beef (Table
4). Interestingly, C. coli was recovered more often from
retail turkey samples than C. jejuni was. Twenty retail meat
samples (18 chicken samples, one turkey sample, and one pork sample)
contained more than one Campylobacter species. Two chicken
samples yielded three species of Campylobacter. Most of
these retail meat samples were collected from different stores or at
different times.
|
Seasonality component.
The prevalence of Campylobacter,
Salmonella, and E. coli in the four meats varied during
the 14-month sampling period (Fig 1).
However, no seasonality component was observed, and these enteric
pathogens were found in retail meats in both warm and cold months.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The present study demonstrated that three major enteric bacterial taxa were present in retail raw meat products obtained from supermarkets in the Greater Washington, D.C., area, including suburban Maryland, over a 14-month period. Chicken carcasses, turkey breasts, beef steaks, and pork chops were used because they are widely available in grocery stores and are representative of meat products that are handled and prepared in the raw state in domestic kitchens. Additionally, these retail meats are often associated with direct hand-to-mouth exposure to enteric pathogens and cross-contamination of the kitchen environment and ready-to-eat foods.
Several studies have indicated that Campylobacter is present in retail raw meats. Raw poultry meats are commonly contaminated with Campylobacter; this is particularly true of chicken products, and the rates of contamination that have been reported are as high as 100% (1, 2). The reported rates of contamination of pork products vary from 1.3% in the United States (10) to 2% in Belgium (18) and 16.9% in Canada (14). The prevalence of Campylobacter in beef is generally low (22, 28). Other studies demonstrated that this pathogen was isolated from only 2 to 10% of the beef samples tested (18, 29). The lower levels of Campylobacter in pork and beef may be due to a lower incidence of these organisms in swine and cattle populations than in poultry, as well as the sensitivity of Campylobacter to atmospheric oxygen and other environmental stresses during transport, processing, and storage of the products tested. Our study also indicated that multiple Campylobacter species are present in raw meats, which has also been observed in other studies (16, 19, 27). More than one species of Campylobacter was identified in 20 meat samples (primarily chicken samples). It is likely that different serotypes or genotypes of the same species (multiple clones) can also be present in one sample, which presents a challenge to molecular subtyping methods used for epidemiological or outbreak investigations. Recent studies have also suggested that coinfection with multiple strains of Campylobacter occurs in 5 to 10% of human cases of acute enteritis (19). Therefore, it is important that more than one bacterial colony per sample be selected for identification and subtyping of Campylobacter. Multiple isolates may be obtained from different isolation steps, such as direct selective plating and selective enrichment, and/or may be identified on the basis of variations in colonial morphology. The Campylobacter isolates recovered in this study are now being analyzed by ribotyping and pulsed-field gel electrophoresis to gain a better understanding of the population genetics of these organisms.
The rates of microbial contamination of retail meats with E. coli in this study ranged from 39% for chicken samples to 12% for turkey samples. The rates of E. coli contamination in the different retail meats were not as dissimilar as the rates observed for Campylobacter contamination. This may have been due to the frequent presence of E. coli in the animal production and food processing environments. In fact, all but three E. coli isolates identified in this study were negative for virulence-associated Shiga toxin or enterotoxin genes. This most likely indicates that the E. coli isolates identified were part of the normal enteric flora that is present in animals and often identified in food production, processing, and distribution environments. The absence of Shiga toxin-producing E. coli strains in the retail meats analyzed in this study is interesting. Several studies have shown that E. coli O157:H7 and other STEC are present in retail meat products, mostly beef products (5, 6, 9, 15, 31). It is likely that STEC could have been recovered from the meat samples tested if an enrichment procedure had been used in this study. However, the overall aim of our research was to investigate general E. coli contamination of retail meats. Also, our study was not designed to determine the levels of microbial contamination in retail meats; hence, our results might not reflect contamination levels.
The reported prevalence of Salmonella in retail meats varies widely in different countries. Salmonella is found less frequently in retail meats in developed countries, although as much as 36% of poultry meat samples were contaminated in a recent study in Belgium (35) and 43% of poultry meat samples were contaminated in a previous study in the United States (4). The rates of Salmonella contamination in pork and beef appear to be much lower, ranging from 0.8 to 10.4% in the United States (10, 32). The difference could be due in part to the types of samples analyzed (whole birds versus steaks; fresh versus frozen). The results of this study indicate that the rates of Salmonella contamination in retail meat samples were low, ranging from 1.9% for beef samples to 4.2% for chicken samples.
The Centers for Disease Control Foodborne Diseases Active Surveillance Network (FoodNet) data indicate that outbreaks and clusters of food-borne infections peak during the warmest months of the year (7). The reasons for this seasonal pattern are not known, but they may include (i) increased prevalence of the pathogens in cattle or other livestock or vehicles of transmission during the summer; (ii) greater human exposure to contaminated foods during the cook-out months; and/or (ii) more improper handling (e.g., temperature abuse) or incomplete cooking of products, such as ground beef, during warm months. Some studies also have shown that the rate of microbial contamination of food products follows the same trend (8, 13, 37). Our results did not provide a clear picture of a seasonality component of microbial contamination of retail meats. It does appear that more meat samples were positive for Campylobacter and E. coli contamination in some of the traditionally warmer months. However, no significant difference in microbial meat contamination was observed when data for warm and cold months were compared. In fact, the rates of Salmonella contamination were higher in cold months than in warm months. This may be explained by the fact that the Salmonella contamination rates in our study were too low to draw any statistically significant conclusions. The findings of this research suggest that future food safety studies focusing on seasonality components may require larger sample sizes and longer analysis periods. An interesting finding of the present study was that the rates of enteric organism contamination of retail meats, particularly chicken carcasses, were significantly different for the four supermarket chains, although all 59 stores of the four chains sold the same product brands. The possible explanations for this finding include differences in store handling practices, sampling times, and product batches. Most studies of retail meats have involved isolation and identification of multiple organisms in different products. We believe that our study was the first study in which the same retail meat samples were examined for Campylobacter, Salmonella, and E. coli contamination in the United States. In a recent study of microbial contamination of pork retail products, the researchers collected samples from six cities in the United States; however, no information concerning differences in store contamination rates in the six cities was given (10). In conclusion, we found that retail raw meats were often contaminated with Campylobacter and E. coli and less often contaminated with Salmonella. The contamination was dependent on the type of meat. Some retail meats were also contaminated with more than one food-borne pathogen. The presence of Campylobacter and Salmonella in retail meats remains a significant public health concern. Our data confirm that raw retail meats may be vehicles for transmitting food-borne diseases. To diminish Campylobacter, E. coli, and Salmonella contamination rates in retail meats, it is critical that risk reduction strategies are used throughout the food chain. These strategies include on-farm practices that reduce pathogen carriage, increased hygiene at both slaughter and meat processing, continued implementation of HACCP systems, and increased consumer education efforts. Additionally, consumption of undercooked meat products and cross-contamination during food handling and preparation must be avoided to ensure food safety at home and in the food service industry. Further research focusing on effective prevention of food-borne illness is essential for developing intervention and mitigation strategies to reduce the presence of food-borne bacterial pathogens at the retail level.
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ACKNOWLEDGMENTS |
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We are indebted to Robert D. Walker from the Division of Animal and Food Microbiology, Center for Veterinary Medicine, U. S. Food and Drug Administration, for his assistance and comments during preparation of the manuscript.
This study was supported in part by a grant from the Maryland Agricultural Experimental Station.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Nutrition and Food Science, University of Maryland, College Park, MD 20742. Phone: (301) 405-1399. Fax: (301) 314-9327. E-mail: jm332{at}umail.umd.edu.
Present address: Department of Health, District of Columbia,
Washington, DC 20020.
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Applied and Environmental Microbiology, December 2001, p. 5431-5436, Vol. 67, No. 12
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.12.5431-5436.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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