Qualitative exposure assessment for Salmonella spp. in shell eggs produced on the island of Ireland

A qualitative exposure assessment for Salmonella in eggs produced on the island of Ireland was developed. The assessment was divided into three main modules (production and packing, distribution and storage, and preparation and consumption), and each of these stages into defined steps in the exposure pathway. In the production and packing stage the initial prevalences of Salmonella in the contents and on the shell of eggs were estimated to be negligible and low respectively. Numbers of Salmonella both in and on eggs were estimated to be low. At each subsequent step in the pathway, qualitative assessments were made of the impact of events on the probability and level of Salmonella contamination on the shells and in the contents of eggs. At the end of each module assessments were combined to give an overall probability and level of Salmonella contamination. In the first two modules the assessment focused on the effect of the duration and temperature of storage on yolk membrane integrity and the likelihood of shell penetration. During the final stage the influence of factors such as safe-handling procedures, pooling practices, consumption patterns and the effectiveness of cooking, on the prevalence and level of Salmonella contamination in a food item at time of consumption was assessed. The outcome of this assessment was an estimate of a low probability and level of Salmonella contamination of egg-containing foods, prepared with eggs produced on the island of Ireland.     

Prevalence of Salmonella spp. in poultry broilers and shell eggs in Korea

This study was conducted to determine the presence of Salmonella spp. in raw broilers and shell eggs in Korea. In total, 135 dozen shell eggs and 27 raw broilers were tested. None of the egg yolks were found to contain Salmonella organisms but Escherichia coli, Escherichia hermanii, and Citrobacter freundii were isolated from egg shells. Salmonella spp. were detected in 25.9% of raw broilers, and Salmonella serotypes isolated from raw broilers were Salmonella Enteritidis, Salmonella Virchow, and Salmonella Virginia. D-values and antibiotic resistance of Salmonella isolates were also investigated. D-values of Salmonella enteritidis, Salmonella Virginia, and Salmonella Virchow in tryptic soy broth at 55 degrees C were 2.36, 2.13, and 0.70 min and 0.53, 0.37, and 0.20 min at 60 degrees C, respectively. All Salmonella isolates showed multiple antibiotic resistance patterns and were resistant to penicillin and vancomycin. One strain of Salmonella Enteritidis showed resistance to 12 antibiotics used in this study.     

Probabilistic model for contamination of egg dishes with Salmonella spp. made from shell eggs produced on the island of Ireland

A quantitative model was constructed to estimate the probability that a serving of food containing eggs produced on the island of Ireland is contaminated with Salmonella spp. The model is based on the prevalence of contaminated eggs at the time of lay and a set of parameters which describe the pooling of eggs in the home and in catering situations. Both external and internal contamination of the eggs by Salmonella spp. was considered. The model estimates that there is a 90% chance that the probability of a serving of food being contaminated is between 0.0043% and 0.038%. Sensitivity analysis demonstrated that egg prevalence drives this low probability and that, at the current level of egg prevalence at the time of lay, pooling of eggs has a minor effect. These results indicate the importance of maintaining the low prevalence of contaminated eggs at the time of lay to minimise the risk of human cases of salmonellosis from consumption of eggs.     

Salmonella Enteritidis in shell eggs: Current issues and prospects for control

Foodborne illness caused by Salmonella spp. is a worldwide problem. In the United States Salmonella Enteritidis is the second most commonly isolated serotype from human illness, and is known to be strongly associated with shell eggs and egg containing products. Eggs can become contaminated internally either by penetration through the shell or directly during formation in the reproductive tract. This review begins with a brief account of the physiology of egg production and the various physical and chemical barriers the egg possesses to prevent bacterial contamination. Factors involved in vertical and horizontal transmission of S. Enteritidis are examined, as well as the role of forced molt in colonization of the hen. Pre- and post-harvest mitigation strategies are also discussed.     

Detection of Salmonella enteritidis in shell and liquid eggs using enrichment and plating

Detection methods using various enrichment and plating media and immunoconcentration for Salmonella enteritidis in shell and liquid eggs were evaluated. For liquid egg samples naturally contaminated with S. enteritidis, pre-enrichment in 225 ml of buffered peptone water with cysteine followed by selective enrichment in 10 ml of tetrathionate broth was the superior, resulting in the detection of S. enteritidis in all samples on six of the seven types of selective agar substrate investigated. This enrichment procedure also enabled detection of S. enteritidis in most of artificially inoculated shell egg and pasteurized liquid egg samples.     

Correlation of eggshell strength and Salmonella enteritidis contamination of commercial shell eggs

Shell quality has been identified as a heritable trait that can be manipulated by genetic selection. Previous research has concluded that many methods of determining shell quality produce variable results. With the development of newer, more precise measuring technologies, shell strength can now be assessed in a consistent, objective fashion. A research project was conducted to determine what role shell strength might play in affecting external Salmonella Enteritidis contamination of egg contents. Visibly clean eggs were collected from an in-line shell egg-processing facility at the accumulator. Eggs were inoculated by dipping in a concentrated suspension of nalidixic acid-resistant Salmonella Enteritidis. After storage, eggs were assessed for shell strength and both external and internal Salmonella Enteritidis contamination. In the first study, there was a significant difference (P < 0.05) in shell strength among the three replicates. No differences between treatments were found for shell strength or Salmonella Enteritidis contamination of contents. In the second study, there were no replicate differences for any of the monitored factors. When rinsate and content samples were enriched, 100% of the rinsates were positive for Salmonella Enteritidis. No content samples were shown to be contaminated with Salmonella Enteritidis during direct plating, but 3 to 5% of the samples from each replicate were positive after enrichment. Correlation analysis of the results from each study found only weak correlations between shell strength and Salmonella Enteritidis contamination on eggshell surface or contents. Within the range of shell strengths recorded in this study, the correlation analysis suggests that shell strength does not play a major role in Salmonella Enteritidis contamination. Further work with eggs that represent a greater range of shell strengths could provide a clearer indication of the interaction of shell strength and Salmonella Enteritidis contamination.     

Preenrichment versus direct selective agar plating for the detection of Salmonella Enteritidis in shell eggs

The relative effectiveness of two methods for the recovery of Salmonella Enteritidis (SE) from jumbo and medium shell eggs was compared. The first method used in the comparison consisted of a preenrichment of the sample, and the second method was developed by the U.S. Department of Agriculture's Animal and Plant Health Inspection Service (APHIS). Three bulk lots of blended, pooled eggs, each containing 220 liquid whole eggs that were thoroughly mixed manually were artificially inoculated with different levels of SE cells between approximately 10(0) and 10(3) CFU/ml. Twenty samples containing the contents of approximately 10 eggs each (by weight) were withdrawn from each of the inoculated bulk lots and incubated for 4 days at room temperature (ca. 23 degrees C). For the APHIS method, each sample was cultured by direct plating onto brilliant green (BG), brilliant green with novobiocin (BGN), xylose lysine desoxycholate (XLD), and xylose lysine agar Tergitol 4 (XLT4) agars. For the preenrichment method, 25-g portions from each pool were enriched in modified tryptic soy broth with 30 mg/liter of FeSO4. After 24 h of incubation, the preenrichments were subcultured to tetrathionate and Rappaport-Vassiliadis broths, and streaked to BG, BGN, bismuth sulfite, XLD, and XLT4 agar plates. SE isolates were confirmed biochemically and serologically. In all of the experiments, the preenrichment method recovered significantly more SE isolates (P < 0.05) of all the phage types and inoculum levels than did the APHIS method. From a total of 539 jumbo egg test portions analyzed, 381 (71%) were SE-positive by the preenrichment method and 232 (43%) were positive by the APHIS method. From a total of 360 medium egg test portions analyzed, 223 (62%) were SE-positive by the preenrichment method and 174 (48%) were positive by the APHIS method. The preenrichment method provided greater sensitivity for the isolation of SE in contaminated egg slurries than did the APHIS method.     

Efficacy of electrolyzed water in inactivating Salmonella enteritidis and Listeria monocytogenes on shell eggs

The efficacy of acidic electrolyzed (EO) water produced at three levels of total available chlorine (16, 41, and 77 mg/ liter) and chlorinated water with 45 and 200 mg/liter of residual chlorine was investigated for inactivating Salmonella Enteritidis and Listeria monocytogenes on shell eggs. An increasing reduction in Listeria population was observed with increasing chlorine concentration from 16 to 77 mg/liter and treatment time from 1 to 5 min, resulting in a maximal reduction of 3.70 log CFU per shell egg compared with a deionized water wash for 5 min. There was no significant difference in antibacterial activities against Salmonella and Listeria at the same treatment time between 45 mg/liter of chlorinated water and 14-A acidic EO water treatment (P > or = 0.05). Chlorinated water (200 mg/liter) wash for 3 and 5 min was the most effective treatment; it reduced mean populations of Listeria and Salmonella on inoculated eggs by 4.89 and 3.83 log CFU/shell egg, respectively. However, reductions (log CFU/shell egg) of Listeria (4.39) and Salmonella (3.66) by 1-min alkaline EO water treatment followed by another 1 min of 14-A acidic EO water (41 mg/liter chlorine) treatment had a similar reduction to the 1-min 200 mg/liter chlorinated water treatment for Listeria (4.01) and Salmonella (3.81). This study demonstrated that a combination of alkaline and acidic EO water wash is equivalent to 200 mg/liter of chlorinated water wash for reducing populations of Salmonella Enteritidis and L. monocytogenes on shell eggs.     

Heat transfer models for predicting Salmonella enteritidis in shell eggs through supply chain distribution

ABSTRACT:  Egg and egg preparations are important vehicles for Salmonella enteritidis infections. The influence of time–temperature becomes important when the presence of this organism is found in commercial shell eggs. A computer-aided mathematical model was validated to estimate surface and interior temperature of shell eggs under variable ambient and refrigerated storage temperature. A risk assessment of S. enteritidis based on the use of this model, coupled with S. enteritidis kinetics, has already been reported in a companion paper published earlier in JFS . The model considered the actual geometry and composition of shell eggs and was solved by numerical techniques (finite differences and finite elements). Parameters of interest such as local ( h ) and global ( U ) heat transfer coefficient, thermal conductivity, and apparent volumetric specific heat were estimated by an inverse procedure from experimental temperature measurement. In order to assess the error in predicting microbial population growth, theoretical and experimental temperatures were applied to a S. enteritidis growth model taken from the literature. Errors between values of microbial population growth calculated from model predicted compared with experimentally measured temperatures were satisfactorily low: 1.1% and 0.8% for the finite difference and finite element model, respectively.     

Prevalence of Campylobacter and Salmonella in raw chicken on retail sale in the republic of Ireland

To assess the current risks to consumers from Campylobacter and Salmonella in raw chicken products sold in the Republic of Ireland, a retail survey was undertaken to define their prevalence. Samples (n = 510) were analyzed using protocols based on ISO 10272-1:2006 and ISO 6579:2002. Processor codes on pack labels showed that 67% of samples were produced in the Republic of Ireland and 25% in the United Kingdom. Salmonella was present in 5.1% of samples, but the eight serovars found caused less than 7% of human salmonellosis reported in the Republic of Ireland. The results suggest that on-farm controls to limit Salmonella infection of broilers have been successful and that in Ireland raw chicken is not a significant cause of salmonellosis in humans. The overall prevalence of Campylobacter spp. was 84.3%. Isolation by the ISO method found 52.7% of samples to be positive, but overgrowth by contaminants was frequently evident. Therefore, in addition to enrichment, an homogenized sample was plated directly onto modified charcoal cefoperazone deoxycholate agar, and this detected a further 31.6%. Speciation of isolates (n = 426) determined that 67% were Campylobacter jejuni and 32% were Campylobacter coli. These species are the most common cause of campylobacteriosis in man. The results indicate that there is a need for poultry producers to introduce interventions to minimize the exposure of consumers in the Republic of Ireland to Campylobacter spp., as has been successfully done for Salmonella.     

Effect of thermoultrasonication on Salmonella enterica serovar Enteritidis in distilled water and intact shell eggs

The combined effects of simultaneous application of ultrasonic waves and heat treatment (thermoultrasonication) on the survival of a strain of Salmonella enterica Enteritidis was studied in both distilled water and intentionally contaminated intact eggs immersed in water. Although minor differences were observed between parameters obtained for thermoultrasonic treatment of bacteria suspended in water and those attached to the shell egg, the thermoultrasonication effects were considered to be of the same level in the range of temperatures assayed (52 to 58 degrees C). This combined process presented a clearly higher killing effect than the heat treatment alone. It decreased the decimal reduction times (D-values) by 80 to 55%, respectively, in the range of temperatures for heat treatment when the organism was suspended in water, which means a 99.5% reduction (5D to >2D) of the original bacterial load versus a 90% reduction for the heat treatment alone. The practical implications of the phenomenon are discussed.     

Sensitivity analysis of Salmonella enteritidis levels in contaminated shell eggs using a biphasic growth model

Salmonella enteritidis (SE) is a common foodbome pathogen, the transmission of which is primarily associated with the consumption of contaminated Grade A shell eggs. In order to estimate the level of SE present in raw shell eggs, it is necessary to consider the protective effects of the egg albumin, which effectively inhibits SE growth in a time- and temperature-dependent manner. In this study, a SE growth model was produced by combining two mathematical equations that described both the extended lag phase of SE growth (food component) and a SE growth model (pathogen component). This biphasic growth model was then applied to various egg handling scenarios based on the farm-to-table continuum, including in-line and off-line processing facilities with consideration of key events in production, processing, transportation, and storage. Seasonal effects were also studied. Monte Carlo simulation was used to characterize variability in temperature and time parameter values influencing the level of SE to which individuals are exposed. The total level of SE consumed was estimated under best, most likely, and time-temperature abusive handling scenarios. The model estimated that, in most cases, there was no SE growth in contaminated eggs handled under most likely practices, because 10-70% of the yolk membrane remained intact. Under abusive handling scenarios, complete loss of yolk membrane integrity frequently occurred by the time eggs reach the distribution phase, followed by subsequent SE growth, which was often quite rapid. In general, the effect of season and processing method (in-line vs. off-line) was minimal. Further sensitivity analysis demonstrated that the initial SE contamination level significantly influenced the final exposure levels only under no-abuse or mildly abusive conditions. The results of our study suggest that, for maximum reduction of SE exposure level, cooling strategies should not only focus on the on-farm or processing phases, but should emphasize the importance of cooling strategies at the distribution and consumer phases of the farm-to-fork continuum.     

Inactivation of Salmonella enterica serovar Enteritidis on shell eggs by ozone and UV radiation

The presence of Salmonella enterica serovar Enteritidis in shell eggs has serious public health implications. Several treatments have been developed to control Salmonella on eggs with mixed results. Currently, there is a need for time-saving, economical, and effective egg sanitization treatments. In this study, shell eggs externally contaminated with Salmonella (8.0 x 10(5) to 4.0 x 10(6) CFU/g of eggshell) were treated with gaseous ozone (O3) at 0 to 15 lb/in2 gauge for 0 to 20 min. In other experiments, contaminated shell eggs were exposed to UV radiation at 100 to 2,500 microW/cm2 for 0 to 5 min. Treatment combination included exposing contaminated eggs to UV (1,500 to 2,500 microW/cm2) for 1 min, followed by ozone at 5 lb/in2 gauge for 1 min. Eggs that were (i) noncontaminated and untreated, (ii) contaminated and untreated, and (iii) contaminated and treated with air were used as controls. Results indicated that treating shell eggs with ozone or UV, separately or in combination, significantly (P < 0.05) reduced Salmonella on shell eggs. For example, contaminated eggs treated with ozone at 4 to 8 degrees C and 15 lb/in2 gauge for 10 min or with UV (1,500 to 2,500 microW/cm2) at 22 to 25 degrees C for 5 min produced 5.9- or 4.3-log microbial reductions or more, respectively, when compared with contaminated untreated controls. Combinations including UV followed by ozone treatment resulted in synergistic inactivation of Salmonella by 4.6 log units or more in about 2 min of total treatment time. Salmonella was effectively inactivated on shell eggs in a short time and at low temperature with the use of a combination of UV radiation and ozone.     

Effects on Salmonella shell contamination and trans-shell penetration of coating hens' eggs with chitosan

Chitosan is a biopolymer with antimicrobial activity and film-forming properties. In this study, the effects on Salmonella shell contamination and trans-shell penetration of coating hens' eggs with chitosan was evaluated. A chitosan was selected from eight types (four non-commercial and four commercial) based on its antimicrobial activity against Salmonella enterica serovar Enteritidis (S. Enteritidis). For this purpose, a contact plate method was developed and chitosans were applied at a concentration of 0.25% (w/v). A commercial type with a molecular weight of 310-375 kDa and a deacetylation degree of 75% that reduced S. Enteritidis by 0.71 log₁₀ colony forming units compared to the control (without chitosan) was selected for further studies. The chitosan was shown to have antimicrobial activity against other egg borne bacteria, i.e., Acinetobacter baumannii, Alcaligenes sp., Carnobacterium sp., Pseudomonas sp., Serratia marcescens and Staphylococcus warneri, and against S. enterica serovar Typhimurium, Escherichia coli and Listeria monocytogenes. The effects of various concentrations of the selected chitosan (0.25%, 1% and 2%) on Salmonella shell contamination and trans-shell penetration were assessed using the agar molding technique. Effective reduction of eggshell contamination could not be demonstrated, but trans-shell penetration was significantly reduced in the presence of a 2% chitosan eggshell coating, with only 6.1% of the eggs being penetrated compared to 24.5% of the uncoated eggs. It was concluded that the 2% chitosan coating has the potential to reduce contamination of egg contents resulting from trans-shell penetration by S. Enteritidis.     

Pasteurization of intact shell eggs

The feasibility of pasteurization for destruction ofSalmonella enteritidisin artificially- inoculated intact shell eggs was investigated. Water-bath and hot air ovens were used for pasteurization of intact shell eggs under different conditions using these two heating methods, either individually or in combination. Eggs pasteurized in a 57°C circulating water-bath for 25 min gave reductions inS. enteritidisATCC 13076 of about 3 log cycles whereas heating at 55°C in a hot air oven for 180 min gave a 5 log reduction ofS. enteritidis. A combin?ation of the two methods (water-bath heating at 57°C for 25 min followed by hot-air heating at 55°C for 60 min) produced 7 log reductions inS. enteritidisATCC 13076 in shell eggs. Examination of lysozyme activity and other physical properties of egg white upon heating indicated that the overall functionality of pasteurized shell eggs are acceptable under the heating conditions defined in this study. This process may be used to produce safe, pasteurized shell eggs.sed     

涂布平板计数法与MPN法定量检测禽肉和蛋中沙门菌的比较

为选择良好的禽肉和鸡蛋中沙门菌定量检测方法 ,通过染菌实验 ,分析比较了涂布平板计数法和MPN法 ,结果表明平板计数法优于MPN法。应用平板计数法检测了 16份鸡蛋和 2 6份禽肉试样。沙门菌检出限分别为 1CFU ml和 10 0CFU g。 16份蛋类试样中均未检出沙门菌。 2 6份鸡肉试样中 ,2 0份为沙门菌阳性 ,阳性率为 77%。其中 9份试样沙门菌数低于检出限 10 0CFU g ,其余试样菌数范围为 1 5× 10 2 ～ 2 5× 10 5CFU g。对 3份 - 2 0℃保存 5d的阳性禽肉试样应用MPN法进行了冷冻前后沙门菌含量的比较分析 ,储存后的菌数比冷冻前略有增加。实验结果表明 ,在食物试样中杂菌污染严重或沙门菌水平较低的情况下 ,平板法不能准确进行沙门菌计数 ,仍需进行MPN定量检测。     

Survey of Salmonella contamination of raw shell eggs used in food service premises in the United Kingdom, 2005 through 2006

This survey was launched after an unusual number of Salmonella Enteritidis outbreaks associated with the use of eggs in food service premises in England and Wales. Between November 2005 and December 2006, 9,528 eggs (1,588 pooled samples of 6 eggs) were collected from 1,567 food service premises in the United Kingdom, most of which (89%) were produced in the United Kingdom. Salmonella was isolated from 6 (0.38%) pools of eggs. Of these, 5 (0.31%) were Salmonella Enteritidis, which were further characterized to phage types (PTs): PT 4 (0.19%), PT 8 (0.06%), and PT 12 (0.06%). Salmonella Mbandaka was also isolated (0.06%). Salmonella was detected from five and one of pooled eggs samples that were produced in the United Kingdom and Germany, respectively; these were from different producers. The study showed evidence of poor egg storage and handling practices in food service premises, in that 55% did not store eggs under refrigerated conditions; 20.7% of eggs had expired "best before" dates or were in use after 3 weeks of lay, indicating poor stock rotation; and 37.1% pooled eggs not intended for immediate service. Eggs are a commonly consumed food that may occasionally be contaminated with Salmonella at different rates, according to their country of origin. The food service sector needs to be aware of this continuing hazard, receive appropriate food safety and hygiene training on storage and usage of raw shell eggs, adopt appropriate control measures, and follow advice provided by national food agencies in order to reduce the risk of infection.     

Efficacy of disinfection of shell eggs externally contaminated with Salmonella enteritidis. Implications for egg testing.

Experimental contamination of the surface of shell eggs by dipping in a culture of Salmonella enteritidis resulted in the presence of Salmonella enteritidis in/on the shells as well as shell membranes but not in the egg content. Disinfection with Lugol's solution, chlorhexidine, ethanol, quarternary ammonium solutions or flaming after dipping in ethanol failed to achieve complete decontamination of the shell and membranes with resulting false positives when eggs were broken for culturing of the content. Dipping eggs for three seconds in boiling water resulted in complete destruction of Salmonella enteritidis in shells and membranes but sometimes caused the eggs to crack. A method of aseptically opening eggs without risk of contaminating the content from the shell or membrane was developed. Salmonella enteritidis deposited in/on the shell and membranes did not multiply during storage of the eggs at 20 degrees C for four weeks, the counts seemed to decrease. No Salmonella enteritidis was detected in the contents of any contaminated eggs.     

中国带壳鸡蛋中沙门氏菌定量危险性评估的初步研究--Ⅰ.危害识别与暴露评估

为控制由食用鸡蛋而导致的沙门氏菌食物中毒 ,利用中国的资料与信息建立了带壳鲜鸡蛋沙门氏菌定量危险性评估模型 ,对中国带壳鲜鸡蛋的沙门氏菌污染情况进行定量评估。模型计算每年以带壳鲜蛋形式被消费的带染鸡蛋数量平均为 2 5× 10 8(5 th～ 95 th百分位点值 :1 9× 10 6～1 1× 10 9)个 ,消费前每个污染鸡蛋中的沙门氏菌菌量平均 70CFU(5 th～ 95 th百分位点值 :14CFU与172CFU) ,该定量危险性评估的框架为中国每年沙门氏菌病暴发的危险性提供了评估依据。