Prevalence of Salmonella Serovars, Listeria monocytogenes, and ...

106 Journal of Food Protection, Vol. 77, No. 1, 2014, Pages 106–111 doi:10.4315/0362-028X.JFP-13-049 Copyright G, International Association for Food Protection

Research Note

Prevalence of Salmonella Serovars, Listeria monocytogenes, and Escherichia coli O157:H7 in Mediterranean Ready-to-Eat Meat Products in Jordan TAREQ M. OSAILI,1* ANAS A. AL-NABULSI,1 REYAD R. SHAKER,1 ZIAD W. JARADAT,1,2 MOHAMMAD TAHA,1 MOHAMMED AL-KHERASHA,3 MERVET MEHERAT,4 AND RICHARD HOLLEY5 1Department of Nutrition and Food Technology; 2Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, Irbid 22110, Jordan; 3Jordan Food and Drug Administration, Amman, Jordan; 4Municipality of Greater Amman, Amman, Jordan; and 5Department of Food Science, University of Manitoba, Winnipeg, Manitoba, Canada R3T 2N2

MS 13-049: Received 6 February 2013/Accepted 26 June 2013

ABSTRACT The presence of Salmonella, Listeria monocytogenes, and Escherichia coli O157:H7 in ready-to-eat (RTE) meat products is considered a major concern for food control authorities worldwide. The aims of this study were to determine (i) the prevalence of Salmonella, L. monocytogenes, and E. coli O157:H7 in Mediterranean RTE chicken and beef (CB) products sold in Jordanian restaurants and (ii) the susceptibility of the isolates to antibiotics. A total of 1,028 samples of various types of RTE CB products (550 RTE chicken and 478 RTE beef products) were analyzed by methods described by the International Organization for Standardization followed by molecular confirmation of the isolates. The VITEK2 automated system was used for testing antibiotic susceptibility of the isolates. The overall prevalence of Salmonella serovars in RTE CB products was 0.5%, with 0.8 and 0.2% in RTE chicken and RTE beef, respectively. The overall prevalence of L. monocytogenes in RTE CB products was 2%, with 2.7 and 1.5% in RTE chicken and RTE beef products, respectively. E. coli O157:H7 was not isolated from any of the tested samples. Multidrug-resistant Salmonella and L. monocytogenes isolates were found. The majority of Salmonella isolates were sensitive to most of the tested antibiotics, and all of the isolates were resistant to more than one antibiotic. Similarly, more than 85% of L. monocytogenes isolates were sensitive to nine antibiotics, and the majority of L. monocytogenes isolates were resistant to fosfomycin and oxacillin.

Ready-to-eat (RTE) food products are those foods that do not require further heat treatment to significantly reduce the microbial load before consumption (8). Examples of traditional RTE meat products in Jordan and in the Mediterranean region are shawirma (beef or chicken meat, sometimes known by other names such as gyro, donair, doner, Do¨ner kebab, and chawarma), beef pastry (a baked food composed of a pastry filled with ground beef meat seasoned with spices), beef kubba (a fried food composed of bulgur wheat and ground beef dough stuffed with ground beef meat seasoned with spices and onion), meat kebab (beef and/or lamb), and beef in pita bread (a baked food composed of a pita bread filled with ground beef meat seasoned with spices). Other popular RTE meat products are roasted chicken and beef or chicken burgers. The presence of a microbiological hazard such as Salmonella, Listeria monocytogenes, and Escherichia coli O157:H7 in RTE meat products is a major concern to food control authorities worldwide. These foodborne pathogens can cause severe illnesses or death to humans, especially high-risk individuals. Major foodborne pathogens (31 * Author for correspondence. Tel: z 962-2-7201000, Ext 22278; Fax: z 962-2-7201078; E-mail: [email protected].

pathogens) cause an estimated 9.4 million cases of foodborne illness, 55,961 hospitalizations, and 1,351 deaths each year in the United States. Fifty percent of the deaths result from consumption of foods contaminated with Salmonella, L. monocytogenes, or E. coli O157:H7 (34). In Jordan, during 2006 and 2007 Salmonella in shawirma from local restaurants caused a total of 1,600 hospitalizations and one death (20). Salmonella, L. monocytogenes, and E. coli O157:H7 have been isolated from various types of RTE meat products in the Mediterranean region (3, 15, 22, 29, 38). In Turkey, Ulukanli et al. (38) isolated E. coli O157:H7 from cooked doner (11.3% of samples) and Kayisoglu et al. (22) isolated Salmonella from cooked beef doner (40% of samples) and cooked chicken doner (80% of samples). In Lebanon, Harakeh et al. (15) isolated Salmonella (7.4% of samples) and E. coli O157:H7 (7.4% of samples) from meat pies and shawirma. In Amman, Jordan, Osaili et al. (29) isolated L. monocytogenes from shawirma (13.3% of samples) and precooked frozen chicken burgers (76.7% of samples). The increased occurrence of multidrug resistance among foodborne pathogens and their resistance to clinically important antibiotics are currently growing global public health concerns (5, 10, 40). Harakeh et al. (15) found

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PREVALENCE OF FOODBORNE PATHOGENS IN RTE MEAT PRODUCTS

that E. coli O157:H7 and Salmonella isolates from meat pies and shawirma were resistant to one or more tested antibiotics. Osaili et al. (29) found that 30% of L. monocytogenes isolates from popular and traditional RTE chicken meat products were resistant to tilmicosin and tetracycline. Assessment of the food safety status and microbiological quality of RTE foods available to consumers in Jordan is one of the major priorities for the Jordan Food and Drug Administration (JFDA), but few studies on the prevalence of foodborne pathogens in RTE food products in Jordan have been published (1, 2, 29, 32). The objectives of the current study were to determine the prevalence Salmonella, L. monocytogenes, and E. coli O157:H7 in Mediterranean RTE meat products sold in restaurants in Jordan and to determine the susceptibility of the isolates to selected antibiotics. MATERIALS AND METHODS Sample collection. One thousand twenty-eight samples of various types of RTE meat products (550 samples RTE chicken and 478 samples of RTE beef products), including chicken or beef shawirma, beef pastry, beef kubba, meat kebab, beef in pita bread, roasted chicken, and chicken or beef burgers, were collected from both large and small restaurants in all 12 Jordan governorates from April through August 2009. The samples were transferred in an insulated container with ice packs to the food laboratories at the Jordan University of Science and Technology, the JFDA, and the Municipality of Greater Amman and analyzed within 24 h. In samples where meat was easily separated from bread, these ingredients were tested separately. When sauce was used, it was tested with the meat. No vegetable samples were collected. Methods of the International Organization for Standardization (ISO) were followed for detection and isolation of Salmonella, L. monocytogenes, and E. coli O157:H7 from all of the samples. Isolation, identification, and confirmation of Salmonella isolates by PCR. Salmonella strains were isolated using the ISO 6579 procedure (18). DNA was extracted from a Salmonella reference strain (ATCC 14028) and suspect Salmonella cells with the Wizard DNA extraction kit (Promega, Madison, WI) according to the manufacturer’s instructions. To confirm the identity of the presumptive Salmonella isolates, a primer pair (59-GTGAAATTATCGCCACGTTCGGGCAA-39, 59-TCATCGCACCGTCAAAGGAACC-39) that targets the invA gene (present in all Salmonella strains) was used (34). DNA amplification was performed according to Rahn et al. (34). All amplifications were conducted in a Veriti thermocycler (Applied Biosystems, Foster City, CA). The reaction products were separated on 2% agarose gels and photographed with a gel documentation system (Gel Doc 2000, Bio-Rad, Hercules, CA). All confirmed Salmonella isolates were sent to Macrogen (Seoul, Korea) for 16S rRNA analysis to identify Salmonella them to serotype. Isolation and identification of L. monocytogenes. L. monocytogenes strains were isolated using the ISO 11290-1 procedure (16, 19). All presumptive isolates were subjected to Gram staining, to oxidase, catalase, hemolysis, motility, and CAMP tests, and to biochemical identification with the Microbact Listeria 12L kit system (Oxoid, Basingstoke, UK). Confirmation of L. monocytogenes isolates by PCR. DNA was extracted from an L. monocytogenes reference strain (ATCC

TABLE 1. Prevalence of Salmonella and Listeria monocytogenes in ready-to-eat chicken and beef products in Jordan No. of samples positive for:

Product

Chicken Shawirma Roasted Burger Total Beef Shawirma Pastry Kubba Kebab In pita bread Burger Total Grand total

Salmonella

Listeria monocytogenes

301 157 20 478

3 1 0 4

12 1 0 13

42 163 115 92 90 48 550 1,028

0 0 1 0 0 0 1 5

1 5 0 2 0 0 8 21

No. of samples

7644) and suspect L. monocytogenes cells with the Wizard DNA extraction kit as per the manufacturer’s instructions. L. monocytogenes–specific primers for the PCR assay were selected based on published nucleotide sequences of the inlA, inlB, inlC, inlJ, actA, hylA, and Iap genes (4, 13, 24, 25). DNA amplification of the inlA, inlB, inlC, and inlJ genes was conducted following the procedure of Liu et al. (24). DNA amplification of the actA, hylA, and Iap genes was performed following the protocols of Cai et al. (4), Mengaud et al. (25), and Furrer et al. (13), respectively. All amplifications were performed in a Veriti thermocycler. The PCR products were separated on 2% agarose gels and photographed with the Gel Doc 2000 system. Isolation of E. coli O157:H7. The ISO 16654 method (17) was followed for isolation of E. coli O157:H7 strains. Antibiotic susceptibility tests. Isolated pathogens were tested for their susceptibility to antibiotics using the VITEK2 automated system (bioMe´rieux S.A., Marcy l’Etoile, France). The AST-P592 card for Staphylococcus aureus was used to test the antibiotic susceptibility of L. monocytogenes isolates because no specific card for Listeria exists, and the AST-GN24 card for gramnegative bacteria was used to test the antibiotic susceptibility of Salmonella isolates. To prepare the microbial inocula for antibiotic susceptibility tests, adequate numbers of colonies were mixed in a sterile saline solution (0.45%) as per the manufacturer’s instructions. The cards were injected with cell suspensions with an integrated vacuum apparatus, sealed, and loaded into the apparatus for incubation (36uC) and analysis. The results were interpreted according to breakpoints recommended by the Clinical and Laboratory Standards Institute (CLSI) (6, 7) and Soussy et al. (36).

RESULTS All of the RTE chicken and beef (CB) samples were analyzed for the presence of Salmonella, L. monocytogenes, and E. coli O157:H7. Five Salmonella enterica serovars were isolated from three types of RTE CB products (Table 1). The overall prevalence of S. enterica in RTE CB products was 0.5%. Two isolates of Salmonella

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TABLE 2. Prevalence of Listeria species other than L. monocytogenes in ready-to-eat chicken and beef products in Jordan No. of samples positive for: L. grayi

L. innocua

L. welshimeri

L. seeligeri

L. ivanovii

Chicken Shawirma Roasted Burger

12 3 0

3 0 0

10 0 0

17 2 0

204 23 0

Beef Shawirma Pastry Kubba Kebab In pita bread Burger Total

5 6 2 0 0 0 28

0 1 0 0 0 0 4

2 5 5 0 0 0 22

1 24 5 1 0 0 50

7 66 47 5 0 1 353

Product

Typhimurium and one isolate of Salmonella Typhi were purified from chicken shawirma, Salmonella Typhimurium was isolated from roasted chicken, and Salmonella Paratyphi was isolated from beef kubba. The prevalence of Salmonella serovars in RTE chicken and RTE beef products was 0.8 and 0.2%, respectively. Salmonella serovars were isolated from 3 (1%) of 301 chicken shawirma samples, 1 (0.6%) of 157 roasted chicken samples, and 1 (0.9%) of 115 beef kubba samples (Table 1). L. monocytogenes was isolated from five types of RTE CB products. The overall prevalence of L. monocytogenes in RTE CB products was 2%. The prevalence of L. monocytogenes in RTE chicken and RTE beef products was 2.7 and 1.5%, respectively. L. monocytogenes was isolated from 12 (4%) of 301 chicken shawirma samples, 1 (0.6%) of 157 roasted chicken samples, 1 (2.4%) of 42 beef shawirma samples, 5 (3.1%) of 163 beef pastry samples, and 2 (2.2%) of 92 meat kebab samples. Listeria grayi and Listeria welshimeri were isolated from RTE CB products at similar rates (2.7 and 2.1%). In contrast, Listeria ivanovii was isolated from RTE CB products at far higher rates than was L. monocytogenes (Table 2). L. ivanovii was isolated from 34.3% of the RTE CB products; it was found in 67.8, 40.9, 40.5, and 14.6% of samples of chicken shawirma, beef kubba, beef pastry, and roasted chicken, respectively. E. coli O157:H7 was not isolated from any of the 1,028 RTE CB products tested. However, non-O157:H7 E. coli was isolated from beef kubba (2% of samples) and beef pastry (1% of samples). The majority of Salmonella serovars isolated were sensitive to most of the tested antibiotics with the exception of nitrofurantoin and trimethoprim-sulfamethoxazole, to which all Salmonella isolates were resistant. Two isolates each of Salmonella Typhimurium from shawirma were resistant to ampicillin, ampicillin-sulbactam, and gentamicin, and one Salmonella Typhi isolate was resistant to ampicillin and ampicillin-sulbactam (Table 3). All of the Salmonella isolates were resistant to more than one antibiotic; Salmonella Typhi was resistant to four antibiotics, and a

shawirma isolate of Salmonella Typhimurium was resistant to five antibiotics. More than 85% of L. monocytogenes isolates were sensitive to nine antibiotics: imipenem, gentamicin, ciprofloxacin, linezolid, teicoplanin, vancomycin, tetracycline, rifampin, and trimethoprim-sulfamethoxazole (Table 4). The majority of L. monocytogenes isolates were resistant to fosfomycin (95% of isolates) and oxacillin (90% of isolates), and 62% of the isolates were resistant to clindamycin or fusidic acid. Multidrug resistance patterns were detected among L. monocytogenes isolates; 57, 14.3, 19, 4.8, and 4.8% of the L. monocytogenes isolates were resistant to three, four, five, six, and eight antibiotics, respectively. DISCUSSION In this study, Salmonella serovars, L. monocytogenes, and other Listeria species were isolated from different types of RTE CB products that are popular in Jordan and East Mediterranean countries. Surprisingly, E. coli O157:H7 was not isolated from any of these products, although this pathogen was isolated previously from raw beef in Jordan at a rate of 7.8% (30). The findings in the current study are promising in comparison with earlier reports on the prevalence of L. monocytogenes in RTE products in Jordan (29, 32). In Amman, Osaili et al. (29) found L. monocytogenes prevalences of 13.3, 76.7, and 30% in chicken shawirma, chicken burger, and chicken sausage, respectively. Further, Osaili et al. (32) found that the prevalence of L. monocytogenes in different types of brined white cheese (soft to semi-hard) was 11.1%. In comparison with data from other Mediterranean countries, the data from the current study suggest that the food safety risk associated with RTE CB products in Jordanian restaurants is lower. In Turkey, Ulukanli et al. (38) found an E. coli O157:H7 prevalence of 11.25% in beef doner kebab, and Kayisoglu et al. (22) found Salmonella prevalences of 40% (12 of 30 samples) in cooked beef doner and 80% (24 of 30 samples) in cooked chicken doner. In Lebanon, Harakeh et al. (15) reported prevalences of 9.5% for E. coli O157:H7 and 7.4% for Salmonella in meat pies and shawirma. In contrast,



109

TABLE 3. MICs and antibiotic sensitivity of Salmonella isolates from ready-to-eat chicken and beef products in Jordan a MIC (mg/ml) Breakpointb Antibiotic

S

Sensitivity, no. (%) of isolates R

Range

S

Ampicillin

#8

$32

Ampicillin-sulbactam

#8, 4

$32, 16

Amikacin Cefazolin Cefoxitin Ceftazidime Ciprofloxacin Cefepime Gentamicin

#16 #8 #8 #8 #1 #8 #4

$64 $32 $32 $32 $4 $32 $16

2 4–16 4–16 1 0.25–2 1 1–16

5 4 3 5 4 5 3

Ertapenem Imipenem Levofloxacin Nitrofurantoin Piperacillin-tazobactam Tobramycin Trimethoprim-sulfamethoxazole

#2 #4 #2 #32 #16, 4 #4 #2, 38

$8 $16 $8 $128 $128, 4 $16 $4, 76

0.5 1–4 0.12–4 128–512 4–8 1 20–320

5 (100) 5 (100) 4 (80)

a b

2–32

I

3 (60) (2 Salmonella Typhimurium and 1 Salmonella Typhi isolate) 3 (60) (2 Salmonella Typhimurium and 1 Salmonella Typhi isolate)

2 (40)

2 (40)

(100) (80) (60) (100) (80) (100) (60)

R

1 (20) 2 (40) 1 (20) 2 (40) (2 Salmonella Typhimurium isolates)

1 (20) 5 (100)

3 (60) 5 (100)

2 (40) 5 (100)

S, sensitive; I, intermediate; R, resistant. From CLSI (6, 7) and Soussy et al. (36).

Vazgecer et al. (39) did not detect Salmonella in 72 chicken doner kebab samples in Turkey. The isolation of Salmonella Typhi and Salmonella Paratyphi from a chicken shawirma and beef kubba sample, respectively, from two different restaurants in the current study is problematic because these organisms are linked to human reservoirs and contaminate food through poor personal hygiene or the use of unsafe water (27). In a 10-year prevalence study of Salmonella, L. monocytogenes, and E. coli O157:H7 in RTE meat and poultry products in the United States, Levine et al. (23) reported Salmonella and L. monocytogenes prevalences similar to those found in the current study, and none of the tested samples were positive for E. coli O157:H7. Meyer et al. (26) reported an L. monocytogenes prevalence of 3% in RTE poultry products in Germany. The presence of foodborne pathogens in RTE CB foods may be attributed to insufficient heat treatment during cooking or to postcooking contamination (14). The absence of E. coli O157:H7 from the tested samples may indicate that the cooking step used in the restaurants was effective for eradicating this bacterium from the products but was not sufficient to eradicate the other two pathogens. E. coli O157:H7 is a relatively heat-sensitive bacterium compared with Salmonella and L. monocytogenes (33). In the current study, Listeria species other than L. monocytogenes were isolated from RTE CB products, especially shawirma, at a very high rate. L. ivanovii, which is rarely considered pathogenic for humans, was the most common Listeria species isolated from the tested products.

Similar to these findings, Osaili et al. (29) found that L. ivanovii was the most common Listeria species isolated from RTE poultry products sold in Jordan; it was found in 67% of chicken shawirma samples. The high prevalence of Listeria in RTE CB products may be due to the ubiquitous nature of this microbe, which can contaminate products in slaughterhouses, before or after cooking, or through food contact surfaces and food handlers (12). In a parallel project (31), we tested two strains of Salmonella Typhimurium isolated from chicken shawirma for their thermal resistance in this product. These strains were more sensitive than expected at 54 to 64uC with D-values of 0.52 to 9.15 min. These results suggest that the risk of Salmonella in shawirma more likely results from inadequate cooking rather than from postcooking contamination, although the isolation of Salmonella Typhi from chicken shawirma in the current study indicates that postcooking contamination may contribute to the risk. Inadequately cooked shawirma itself may be a health risk to customers, and partially cooked slices could transfer Salmonella to cooked slices. Most Salmonella isolates in the current study were sensitive to the majority of antibiotics tested; however, resistance was noted, and some isolates were resistant to more than two antibiotics, especially the Salmonella Typhi and Salmonella Typhimurium isolates from chicken shawirma. Similar resistance patterns have been previously reported for Salmonella. Harakeh et al. (15) found that 86 and 57% of the Salmonella isolates from meat-based fast food in Lebanon were resistant to trimethoprim-sulfamethoxazole and gentamicin, respectively. Thai et al. (37) found

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TABLE 4. MICs and antibiotic sensitivity of Listeria monocytogenes isolates from ready-to-eat chicken and beef products in Jordan a MIC (mg/ml)

Sensitivity

Breakpointb

Sample isolates, no. (%) of isolates

Antibiotic

S

R

Range

L. monocytogenes (ATCC 7644)

Benzylpenicillin Oxacillin Imipenem Gentamicin Ciprofloxacin Erythromycin Clindamycin Linezolid Teicoplanin Vancomycin Tetracycline Fosfomycin Fusidic acid Rifampin Trimethoprim-sulfamethoxazole

#0.25 #2 #4 #4 #1 #0.5 #0.5 #4 #8 #2 #4 #32 #2 #1 #0.5, 9.5

.16 $4 $16 $8 $4 $8 $4

0.03–0.5 0.25–4 1 0.5 0.5–2 0.25–4 0.25–8 1–4 0.5 0.5–2 1–16 128 0.5–16 0.5–32 10

S R S S S S S I S S S R I S S

a b

$32 $16 .32 .16 $4 $4, 76

S

16 2 21 21 20 15 8 20 20 19 19 1 0 18 20

(76) (10) (100) (100) (95) (71) (38) (95) (95) (90) (90) (5) (85.5) (95)

I

5 0 0 0 0 3 0 0 0 1 0 0 8 0 1

(24)

(14.5)

(5)

(38) (5)

R

0 19 0 0 1 3 13 1 1 1 2 20 13 3 0

(90)

(5) (14.5) (62) (5) (5) (5) (10) (95) (62) (14.5)

S, sensitive; I, intermediate; R, resistant. From CLSI (6, 7) and Soussy et al. (36).

that 68 and 54.5% of Salmonella Typhimurium isolates from retail pork and chicken meat in Vietnam were resistant to ampicillin and gentamicin, respectively, but all of the 22 Salmonella Typhimurium isolates were sensitive to ceftazidime. Kakatkar et al. (21) found that Salmonella Typhimurium isolates from Indian foods were characterized by their sensitivity to ampicillin and ciprofloxacin. The antibiotic resistance patterns of L. monocytogenes isolates in the current study were similar to those reported in the literature. Zhang et al. (41) reported that L. monocytogenes isolates from RTE meat products in the United States were sensitive to gentamicin and trimethoprim. Fallah et al. (11) found that L. monocytogenes isolates from RTE poultry products sold in Iran were sensitive to ciprofloxacin and tetracycline, and Conter et al. (9) found that L. monocytogenes food isolates were sensitive to imipenem, gentamicin, teicoplanin, and fosfomycin and resistant to fusidic acid. In the current study, isolates resistant to one antibiotic were more common than isolates with multidrug resistance. Conter et al. (9) reported that 8.3, 2.5, and 0.8% of L. monocytogenes isolates were resistant to one, two, and five antibiotics, respectively. In summary, the prevalences of Salmonella, L. monocytogenes, and E. coli O157:H7 in RTE CB products in Jordan were low compared with those in other countries in the region, as previously was published; however, obligatory implementation of strict food safety regulations in restaurants that sell high-risk RTE CB products should be continuously enforced and monitored by regulatory agencies in Jordan for food safety, and improvements are always needed. Osaili et al. (28) found that food workers in restaurants in Jordan had inadequate knowledge of some aspects of food safety.

ACKNOWLEDGMENTS The authors thank the Higher Council for Science and Technology and the Deanship of Scientific Research at Jordan University of Science and Technology for funding this project.

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