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ORIGINAL ARTICLE
Int J Env Health Eng 2012,  1:48

Microbial quality and prevalence of Salmonella and Listeria in eggs


1 Department of Pharmaceutical Biotechnology, Faculty of Pharmacy, Isfahan University of Medical Sciences (IUMS), Isfahan, Iran
2 Infectious Disease and Tropical Medicine Research Center, IUMS, Isfahan, Iran
3 Department of Microbiology, School of Medicine, IUMS, Isfahan, Iran
4 Food Security Research Center, IUMS, Isfahan, Iran

Date of Web Publication31-Dec-2012

Correspondence Address:
Mohammad Jalali
Infectious Disease and Tropical Medicine Research Center, Isfahan University of Medical Sciences, Isfahan
Iran
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Source of Support: Isfahan University of Medical Sciences, Conflict of Interest: None


DOI: 10.4103/2277-9183.105347

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  Abstract 

Aims: This study was undertaken to determine the microbial quality and the prevalence of Salmonella and Listeria in table eggs in Isfahan, Iran.
Materials and Methods: A total of 525 samples were randomly collected from various shops in Isfahan, Iran. Microbial quality of eggs evaluated by coliform count and total bacterial viable counts. Also, detection of Listeria and Salmonella in egg contents and on eggs shells was performed.
Results: The mean of total viable bacteria and coliform counts in the egg contents were 3.95 × 10 4 CFU/g and 4.94 × 10 3 CFU/g, respectively. Salmonella and Listeria were not found on the shell or content of eggs. Enterobacteriaceae families were found in 357 of 525 (68.28%) and 276 of 525 (52.44%) of egg shell and egg content samples, respectively. Moreover, Pseudomonas aeruginosa was isolated from 175 (33.41%) and 144 (25.37%) of egg shell and egg content, respectively. The isolated Enterobacteriaceae were included: Enterobacter aerogenes, Escherichia coli, Klebsiella pneumoniae, Buttiauxella agrestis, Cedecea lapagei, Cedecea davisae and Erwinia herbicola.
Conclusion: The findings of the present study indicate although Salmonella and Listeria were not found in egg samples; however, there is an urgent need to improve the hygienic level of consumed eggs.

Keywords: Coliform, egg, enterobacteriaceae, listeria, salmonella


How to cite this article:
Mahdavi M, Jalali M, Safaei HG, Shamloo E. Microbial quality and prevalence of Salmonella and Listeria in eggs. Int J Env Health Eng 2012;1:48

How to cite this URL:
Mahdavi M, Jalali M, Safaei HG, Shamloo E. Microbial quality and prevalence of Salmonella and Listeria in eggs. Int J Env Health Eng [serial online] 2012 [cited 2018 Apr 20];1:48. Available from: http://www.ijehe.org/text.asp?2012/1/1/48/105347


  Introduction Top


Eggs that constitute several dishes or foods consumed and are considered as good quality source of protein, have served as vehicles for numerous enteropathogens microorganisms. [1],[2] The well-known enteric pathogens particularly  Salmonella More Details,  Escherichia More Details coli, Campylobacter spp. and Listeria spp. have been isolated from table eggs and their contents. [3],[4],[5] In addition, most of these bacteria have been responsible for numerous egg-borne epidemics globally. [6],[7],[8],[9] Other members of the family of Enterobacteriaceae such as Pseudomonas spp., Citrobacter spp., Alcaligenes spp., and Klebsiella spp. have all been isolated from whole or cracked eggs with a potential to cause spoilage and enter the food chain through table eggs causing infection in consumers. [2],[10],[11],[12],[13]

 Salmonellosis More Details constitutes a major public health burden and represents a significant cost in many countries. Salmonella and in particular Salmonella enteritidis outbreaks in humans are very often linked to the consumption of contaminated eggs or food containing eggs. [14],[15],[16] The bacterium infects the eggs by either vertical transmission during development of the egg within the ovary or horizontal transmission through trans-shell contamination. [15],[17],[18],[19] Listeria monocytogenes considered an important foodborne pathogen causes severe disease with high mortality in human. [20] The presence of L. monocytogenes has been reported from a wide variety of foods including eggs. [21],[22] Also, many reports clearly show that eggs are a suitable substrate for the growth of L. monocytogenes. [23] The presence of Listeria and Salmonella in other foods in Iran has been reported. However, there are no data on occurrences of both pathogens in eggs. [24],[25] There are also limited data available on microbial quality of table eggs in Iran. Therefore, the objective of this study was to determine the microbial quality and also the occurrence of Listeria and Salmonella in consumption eggs in Isfahan, Iran.


  Materials and Methods Top


Eggs samples

Overall, a total of 525 chicken eggs samples were randomly collected from various super markets in Isfahan, Iran over a period of one year (July 2009-July 2010). Each sample assessed for the total bacterial viable count and coliform count by pour plate method. Also, detection of Listeria and Salmonella were performed.

Swab sampling of eggs

A sterile swab soaked in saline was applied to the surface of each egg shell and swabs were then dipped into 10 mL of saline. The contents of the saline were mixed thoroughly using a vortex mixer and subsequently inoculated into appropriate bacteriological media for detection of Salmonella and Listeria.

Sampling of egg contents

Each egg sample was dipped in 90% ethanol for 5 min after which the pointed end of egg was famed for 5-10 s with a Bunsen burner. A sterile scalpel blade was used to make a small hole on the shell through which the contents were transferred into a stomacher bag. The egg contents (yolk and albumen) in each pool were then blended for 30 s after which the mixture was used to inoculate appropriate bacteriological media.

Salmonella detection

Samples were examined for the presence of Salmonella by the Iranian National Standards method No. 1810 recommended by the Institute of Standards and Industrial Research of Iran (ISIRI) for the isolation of Salmonella. Each egg's content was mixed thoroughly and then 25 mL of egg contents or one ml of saline containing swabs were added to 225 and 25 mL of Buffered Peptone Water (BPW, Merck, Germany) respectively and incubated at 37°C overnight as pre-enrichment. One milliliter of the cultures were transferred to 9 mL of selenite cystine broth (Merck; Germany) and incubated at 37°C for 24 h for selective enrichment. The cultures were then streaked onto xylose lysine deoxycholate (XLD, Merck; Germany) agar and incubated at 37°C for 24-48 h. The plates were observed for typical Salmonella-like colonies. [26]

Listeria detection

Samples were analyzed for the presence of Listeria spp. using selective enrichment and isolation protocol, recommended by United States Department of Agriculture (USDA). [27] Each egg's content was mixed thoroughly and then 25 mL of egg contents or one ml of saline containing swabs were added to 225 and 25 mL of University of Vermont Media (UVM) I respectively and incubated at 37°C overnight as pre-enrichment. Then, 1 mL of the cultures were transferred to 9 mL of UVM II (Fraser broth) and incubated at 37°C for 24-48 h for selective enrichment. The cultures were then streaked onto PALCAM (Merck; Germany) agar and supplemented with PALCAM Selective Supplement (HC784958 Merck; Germany) and incubated at 37°C for 24-48 h. The plates were observed for typical Listeria-like colonies.

Total bacterial viable and coliform count

Total bacterial viable count (TVC) and total coliform count (TCC) was performed using pour plate method. The egg samples were diluted by tenfold serial dilution in 0.1% sterile buffered peptone water (Oxoid; UK). From each dilution, one ml aliquot was added to Nutrient Agar (Merck; Germany) and Violet Red Bile Agar (VRBA, Merck; Germany) for TVC and TCC respectively. All plates were then incubated at 37°C for 72 h. Colonies were counted using a plate counter and the results expressed as CFU/ mL of egg samples. The VRBA plates were examined for typical coliform colonies (violet colonies) and colorless Lactose-negative enterobacteria colonies. Then, at least five suspected colonies were subcultured on Trypton Soy Agar and incubated at 37°C for 24 h. All isolates were subjected to standard biochemical tests such as Gram staining, catalase test, Oxidase test, SIM test, TSI test, OF test, acid production from glucose, manitol, rhamnose, xylose, and MR/VP test. For further confirmations of Psedumonas auroginosa colonies other biochemical reactions, nitrate reduction, and growth on Cetrimide agar were performed according to the Bergey's Manual of Systematic Bacteriology.


  Results Top


As shown in [Table 1], 213 (40.6%) of samples had a TVC of 0-10 CFU/g and TVC of 10 6 -10 7 CFU/g found only in 1 (0.2%) of egg samples. TVC of 10, 10-10 2 , 10 2 -10 3 , 10 3 -10 4 , 10 4 -10 5 , 10 5 -10 6 , and 10 6 -10 7 CFU/g were in 213 (40.6%), 15 (2.9%), 27 (5.1%), 108 (20.6%), 116 (22.1%), 45 (8.6%), and 1(0.2%) of samples, respectively. Also in [Table 1], the distribution of total coliform count (TCC) of egg samples is shown. TCC of 10, 10-10 2 , 10 2 -10 3 , 10 3 -10 4 , 10 4 -10 5 , 10 5 -10 6 and 10 6 -10 7 CFU/g were in 447 (85.14%), 24 (4.57%), 33 (6.29%), 12 (2.29%), 7 (1.33%), 0(0%), and 2(0.38%) of samples, respectively.
Table 1: Distribution of total bacterial viable count (TVC) and total coliform count (TCC) of egg samples

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The prevalence of bacterial species isolated from the shell and content of consumed eggs are shown in [Table 2]. Enterobacter erogenes, E. coli, Klebsiella pneumoniae, Buttiauxella agrestis, Cedecea lapagei, Cedecea davisae,  Erwinia herbicola Scientific Name Search  and Psedumonas aeruginosa were the most common isolated species [Table 2]. Pseudomonas was the only non- Enterobacteriaceae member identified. In this research P. aeruginosa was the most frequently isolated species on egg shells and contents. This bacterium isolated from 175 (33.41%) and 144 (27.32%) of egg shells and contents, respectively.
Table 2: The prevalence of bacterial species from the shell and content of consumed eggs

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  Discussion Top


The mean total viable bacteria and coliform counts of tested eggs were 4.31 × 10 4 and 1.46 × 10 3 CFU/g, respectively. 163 (30.9%) of egg samples had TVC more than FDA standard. These numbers are more than the FDA total and coliform standard count of eggs that is 5×10 3 CFU/g for total count and 1 CFU/g for coliform count. [28] Since the TCC of more than 1 CFU/g is unacceptable, 79 (15%) of the samples are considered above the standard limits. The presence of coliform indicates the possibility of fecal contamination. Coliform has been used as an indicator microorganism to determine the microbial quality and safety of the food. They are defined as rod-shaped Gram-negative nonspore forming bacteria that universally present in large numbers in the faeces of warm-blooded animals. While coliforms are themselves not normally causes of serious illness, they are easy to culture and their presence is used to indicate that other pathogenic organisms of faecal origin may be present.

The presence and population of bacteria on shell and content eggs is an important factor for evaluating the efficacy of washing and packaging as well as the quality and safety of the final product. Enterobacteriaceae, a bacterial family that includes the important human pathogens of Salmonella and Shigella, are known to contaminate the shell egg processing environment. High levels of these bacteria in the processing plant can signal inadequate sanitation. However, little is known about the number of genera and species that contribute to contamination of eggs. [29],[30]

Recently Michael Musgrove and Deana Jones (2009) found 100% prevalence for Enterobacteriaceae on nests run carts at one plant and 80% at the other. They were also reported the presence of Escherichia, Enterobacter, Klebsiella, Salmonella, and Pseudomonas. Knowing bacterial species are vital pieces of information in developing strategies to reduce and remove bacterial contamination. This work demonstrated that nest run egg carts serve as reservoirs for Enterobacteriaceae in the shell egg processing environment. These findings helped egg industry and regulators agents to encourage development of better sanitation procedures or the use of more easily cleaned shelving materials.

P. aeruginosa is an opportunistic, nosocomial human pathogen of immunocompromised individuals and typically infects the pulmonary tract, urinary tract, burns, wounds, and also causes other blood infections in humans. [31] In addition, bacteria of the genus Pseudomonas have been shown to more readily penetrate into whole eggs of poor shell quality. [32] Not surprising, at the present study, P. aeruginosa were prevalent on both egg content and egg shell. Since the Pseudomonas spoilage is the most frequent spoilage in stored eggs, this can raise a concern on safety and quality of eggs in Iran. Different researchers reported the role of penetration of bacteria through the egg shell with associated membranes and on whole egg contamination. In our research, as expected, contamination of egg shell is higher than egg content. This finding indicated the shorter shelf life for eggs especially in poor storage condition.

Musgrove and Jones (2009) reported Escherichia and Enterobacter were present most often compared to other member of Enterobacteriaceae in swab samples from the cart shelves. Furthermore, Adesiyun et al. (2006) reported 71 (38.6%) of 184 composite eggs (shells, yolk/albumen or both) samples were positive for enteric microbes, other than E. coli, Salmonella, Campylobacter spp., and Listeria spp. Enterobacter spp. and Klebsiella spp. were isolated from 15 (8.2%) and 14 (7.6%), respectively, of pooled egg shells alone and from 6 (3.3%) and 3 (1.6%), respectively, of egg content samples alone. [33] In this work, Enterobacter aeruginosa, E. coli, and Klebsiella pneumoniae Scientific Name Search  were also found in 132 (25.12%), 32 (6.1%), and 13 (2.44%) of swab samples, respectively and from 123 (23.41%), 9 (1.71%) and none of egg contents, respectively [Table 2]. Chousalkar et al. (2010) studied the prevalence of Salmonella and E. coli from the surface of egg shells, egg shell membranes or pores, and internal contents from unwashed eggs collected from commercial caged layer farms in Australia. [34] Similar to our findings Salmonella spp. was not detected either in internal egg contents or egg shell surface. Seven percent E. coli were isolated from the egg shell surface. Two percent E. coli strains were also isolated from shell crush. However, unlike our study, the internal contents of eggs appeared to be sterile.

The results of this work are confirmed contamination of Isfahan egg samples, while there were not found Salmonella spp. Salmonellosis is one of the most common causes of foodborne diarrheal disease worldwide and remains a major public health problem in many parts of the world. [35] Salmonella enterica subspecies enterica serovar enteritidis (S. enteritidis) is the world-leading cause of salmonellosis and is often implicated in over 60% of cases of human salmonellosis in Europe. [36] The majority of human cases are caused by only a few nontyphoidal serovars. For instance, approximately 60% of human cases reported to the CDC in 1995 were caused by four serovars, including Salmonella enteritidis (24.7%), S. typhimurium (23.5%), S. newport (6.2%), and S. heidelberg (5.1%). [37] In spite of the fact that food poisoning has often been found after consuming eggs in different parts of the world, little research has been done on quantitative determination of Salmonella in naturally contaminated eggs so far. Investigations have showed that the concentration of Salmonella spp. in most cases is very low, from one to ten cells in one egg despite keeping the eggs at the room temperature for 7 days. [38]

Based on investigation of 525 eggs purchased from Isfahan shops, Salmonella spp. was not found on the shell or inside the eggs. The findings give the impression that eggs are relatively rarely contaminated by Salmonella spp. on the surface. Research carried out in USA and Great Britain showed a very low level of egg contamination even when the eggs came from flocks infected with Salmonella spp. In contrast to our results, the Public Health Laboratory Service in Great Britain has investigated eggs coming from farms whose eggs had earlier caused food poisoning and demonstrated that approximately 0.1% of contents were positive for Salmonella. [38] Radkowski (1990) examined 700 eggs from Poland, and in 400 eggs coming from state farms, Salmonella spp. was found on the shell of only one egg (0.25%) and in 300 eggs coming from individual farms it was found on the shells of three eggs (1%). [39]  Listeria monocytogenes Scientific Name Search nes has been recognized as a human pathogen for decades and is known to be an important foodborne pathogen. There have been no documented foodborne L. monocytogenes illnesses due to the consumption of eggs or egg products, even though the bacterium has been isolated from faeces, body fluid, and oviducts of asymptomatic laying hens. [22] In contrast to this study, Rivoal et al. 2010, was detected L. monocytogenes in 25 of the 144 raw egg samples collected in France. In addition they proposed contamination of raw egg products appeared to be season dependant and was higher during summer and winter than during autumn. In Japan, Miho et al. (2009) was also isolated L. monocytogenes from 2 of 487 (0.4%) unpasteurized liquid whole egg samples in 1993 and 1994, and 2 of 316 (0.6%) unpasteurized liquid whole egg samples. Sayed et al. (2009) in Egypt in contrast to present study reported that egg shells were contaminated by Listeria up to7% while similar to our finding, none of egg contents were contaminated, concluding that egg shell was more subjected to contamination with L. monocytogenes than egg content. [40]

The absence of Listeria and Salmonella in eggs investigated in this study is in agreement with the finding of Ghasemian Safaei et al. (2011) who recently reported no contamination of Salmonella spp. and Listeria spp. in 100 eggs. [41] In spite of the fact that we have reported Listeria spp. and Salmonella spp. contamination of various foods in the same region it is not clear that why eggs are not contaminated by Listeria spp. and Salmonella spp. [24],[25]


  Acknowledgements Top


This project was funded by the deputy of research of Isfahan University of Medical Sciences, Isfahan, Iran.

 
  References Top

1.Blumenthal D. From the chicken to the egg. FDA Consumer 1990 (April), 7-10. Ministry of Agriculture, Fisheries and Food (MAAF) (2000). Eggs and poultry meat frequently asked question. Available from: http://www.maV.-gov.uk/foodrin/poultry/epfaq.htm [Last accessed on 10. 03 2012]  Back to cited text no. 1
    
2.Papadopoulou C, Dimitriou D, Levidiotou S, Gessouli H, Panagiou A, Golegou S, et al. Bacterial strains isolated from eggs and their resistance to currently used antibiotics: Is there a health hazard for consumers? Comp Immunol Microbiol Infect Dis 1997;20:35-40.  Back to cited text no. 2
[PUBMED]    
3.Adesiyun A, OYah NV, Seepersadsingh N, Rodrigo S, Lashley V, Musai L. Microbial health risk posed by table eggs in Trinidad. Epidemiol Infect 2005;133:1049-56.  Back to cited text no. 3
    
4.Farber JM, Daley E, Coates F. Presence of Listeria spp. in whole eggs and wash water samples from Ontario and Quebec. Food Res Int 1992;25:143-5.  Back to cited text no. 4
    
5.Hope BK, Baker R, Edel ED, Hogue AT, Schlosser WD, Whiting R, et al. An overview of the Salmonella enteritidis risk assessment for shell eggs and egg products. Risk Anal 2002;22:203-18.  Back to cited text no. 5
[PUBMED]    
6.Centers for Disease Control (CDC), Update: (1990). S. enteritidis infections and grade a shell eggs, United States 1989;MMWR 38:877-80.  Back to cited text no. 6
    
7.Mazurek J, Holbert L, Parrish MK, Salehi E. Raw eggs-lessons learned from an outbreak of Salmonella serotype enteritidis infection associated with meringue pie. J Pub Health Manag Prac 2005;11:201-7.  Back to cited text no. 7
[PUBMED]    
8.Rocourt J, BenEmbarek P, Toyofuku H, Schlundt J. Quantitative risk assessment of Listeria monocytogenes in ready-to-eat foods: The FAO/WHO approach. FEMS Immunol Med Microbiol 2003;35:263-7.  Back to cited text no. 8
[PUBMED]    
9.Todd EC. Risk assessment of use of cracked eggs in Canada. Int J Food Microbiol 1996;30:125-43.  Back to cited text no. 9
[PUBMED]    
10.Ibeh IN, Izuagbe YS. An analysis of the microflora of broken eggs used in confectionery products in Nigeria and the occurrence of enterotoxigenic Gram-negative bacteria. Int J Food Microbiol 1986;3:71-7.  Back to cited text no. 10
    
11.Jones DR, Musgrove MT, Northcutt JK. Variation in external and internal microbial populations in shell eggs during extended storage. J Food Protect 2004;67:2657-60.  Back to cited text no. 11
[PUBMED]    
12.Musgrove MT, Jones DR, Northcutt JK, Cox NA, Harrison MA. Identification of Enterobacteriaceae from washed and unwashed commercial shell eggs. J Food Protect 2004;67:2613-6.  Back to cited text no. 12
[PUBMED]    
13.Wadstrom T, Ljungh A. Aeromonas and Plesiomonas as food and waterborne pathogens. Int J Food Microbiol 1991;12:303-12.  Back to cited text no. 13
    
14.Davies R, Breslin M. Environmental contamination and detection of Salmonella enterica serovar enteritidis in laying flocks. Vet Rec 2001;149:699-704.  Back to cited text no. 14
    
15.Van Immerseel F, De Buck J, Boyen F, Pasmans F, Bertrand S, Collard JM, et al. Salmonella dans la viande de volaille et dans les oeufs, un danger pour le consommateur qui demande la mise en place d′un programme de lutte efficace. Journal of Veterinaries Medicine 2005;149:34-48.  Back to cited text no. 15
    
16.Collard JM, Bertrand S, Dierick K, Godard C, Wildemauwe C, Vermeersch K, et al. Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect 2007;24:1-11.  Back to cited text no. 16
    
17.Kinde H, Shivaprasad HL, Daft BM, Read DH, Ardans A, Breitmeyer R, et al. Pathologic and bacteriologic findings in 27-week-old commercial laying hens experimentally infected with Salmonella enteritidis, phage type 4. Avian Dis 2000;44:239-48.  Back to cited text no. 17
[PUBMED]    
18.WHO FAO, World Health Organization, Food and Agriculture Organization of the United Nations, 2002. Risk assessments of Salmonella in eggs and broiler chickens, an interpretative summary. Microbiological Risk Assessment Series 1.  Back to cited text no. 18
    
19.Davies R, Breslin M. Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Vet Rec 2003;152:283-7.  Back to cited text no. 19
[PUBMED]    
20.Farber JM, Peterkin PI. Listeria monocytogenes, a foodborne pathogen. Microbiol Rev 1991;55:476-511.  Back to cited text no. 20
[PUBMED]    
21.Miho O, Miyuki N, Nobuhiro S. Detection of Listeria monocytogenes in Commercially Broken Unpasteurized Liquid Egg in Japan. J Food Protect 2009;72:178-81.  Back to cited text no. 21
    
22.Rivoal K, Quéguiner S, Boscher E, Bougeard S, Ermel G, Salvat G, et al. Detection of Listeria monocytogenes in raw and pasteurized liquid whole eggs and characterization by PFGE. Int J Food Microbiol 2010;138:56-62.  Back to cited text no. 22
    
23.Hwang C, Marmer BS. Growth of Listeria monocytogenes in egg salad and pasta salad formulated with mayonnaise of various pH and stored at refrigerated and abuse temperatures. Food Microbiol 2007;24:211-8.  Back to cited text no. 23
    
24.Jalali M, Abedi D. Prevalence of Listeria species in food products in Isfahan, Iran. Int J Food Microbiol 2008;122:336-40.  Back to cited text no. 24
[PUBMED]    
25.Jalali M, Abedi D, Pourbakhsh A, Ghoukasian K. Prevalence of Salmonella Spp. In Iran raw and cooked foods in Isfahan, Iran. J Food Saf 2008;28:442-52.  Back to cited text no. 25
    
26.Iranian Standard Organization. No 1810: Method recommended for the isolation of Salmonella from food. 1995.  Back to cited text no. 26
    
27.McClain D, Lee WH. Development of USDA-FSIS method for isolation of Listeria monocytogenes from raw meat and poultry. J Assoc Off Anal Chem 1988;71:660-4.  Back to cited text no. 27
[PUBMED]    
28.Gilbert RJ, de Louvois J, Donovan T, Little C, Nye K, Ribeiro CD, et al. Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale. Commun Dis Public Health 2000;3:163-7.  Back to cited text no. 28
[PUBMED]    
29.Musgrove MT, Jones DR, Shaw JD, Sheppard M, Harrison MA. Enterobacteriaceae and related organisms isolated from nest run cart helves in commercial shell egg processing facilities. Poultry Sci 2009;88:2113-7.  Back to cited text no. 29
[PUBMED]    
30.Jones DR, Musgrove MT. Identification of nterobacteriaceae on vacuum loaders in shell egg processing. Poultry Sci 2008;87:1678-81.  Back to cited text no. 30
    
31.Balcht A, Smith R. Pseudomonas aeruginosa: Infections and treatment. Informa Health Care 2006;1:83-84.  Back to cited text no. 31
    
32.De Reu K, Grijspeerdt K, Messens W, Heyndrickx M, Uyttendaele M, Debevere J, et al. Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella enteritidis. Int J Food Microbiol 2006;112:253-60.  Back to cited text no. 32
[PUBMED]    
33.Adesiyun A, OYah NV, Seepersadsingh N, Rodrigo S, Lashley V, Musai L. Frequency and antimicrobial resistance of enteric bacteria with spoilage potential isolated from table eggs. Food Res Int 2006;39:212-19.  Back to cited text no. 33
    
34.Chousalkar K, Flynn P, Sutherland M, Roberts JR, Cheetham BF. Recovery of Salmonella and Escherichia coli from commercial egg shells and effect of translucency on bacterial penetration in eggs. Int J Food Microbiol 2010;142:207-13.  Back to cited text no. 34
    
35.Mead PS, Slutsker L, Dietz V, MaCraig LF, Bresee JS, Shapiro C, et al. Food related illness and death in the United States. Emerg Infect Dis 1999;5:607-34.  Back to cited text no. 35
    
36.Thorns CJ. Bacterial food-borne zoonoses. Rev Sci Tech 2000;19:226-39.  Back to cited text no. 36
[PUBMED]    
37.CDC. Salmonella surveillance: Annual tabulation summary, 1993-1995. Atlanta: US Department of Health and Human Services, CDC; 1996.  Back to cited text no. 37
    
38.Radkowski M. Occurrence of Salmonella spp. in consumption eggs in Poland. Int J Food Microbiol 2001;64:189-91.  Back to cited text no. 38
[PUBMED]    
39.Radkowski M. Wyste¸powanie palÇeczek Salmonella wjajach kurzych. Med Wet 1990;46:331-6.  Back to cited text no. 39
    
40.Sayed M, Abdel-Azeem M, Farghaly M, Hassanein R. Using of PCR assay for identification of Listeria monocytogenes recovered from table eggs. Vet World 2009;2:453-5.  Back to cited text no. 40
    
41.Ghasemian Safaei H, Jalali M, Hosseini A, Narimani T, Sharifzadeh A, Raheimi E. The prevalence of bacterial contamination of table eggs from retails markets by Salmonella spp., Listeria monocytogenes, Campylobacter jejuni and Escherichia coli in Shahrekord, Iran. Jundishapur J Microbiol 2011;4:249-53.  Back to cited text no. 41
    



 
 
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