Salmonella enteritidis and eggs

Elimination of Salmonella enterica serovar Typhimurium in artificially contaminated eggs through correct cooking and frying procedures

Eliminação de Salmonella enterica sorovar Typhimurium em ovos contaminados artificialmente por procedimentos corretos de cozimento e fritura

Geovana Dagostim Savi; Tiago Bortolotto; Lutiana Roque Simões; Tatiana Barichello *

Salmonellosis is a serious foodborne disease associated with the presence of bacteria in eggs or foods containing raw eggs. However, the use of appropriate procedures of cooking and frying can eliminate this contamination. There are few studies on the elimination of contamination of Salmonella in hens' eggs through typical frying procedures, especially for Salmonella enterica serovar Typhimurium (or S. typhimurium). The aim of this study was to determine the appropriate conditions for cooking and frying hens' eggs artificially contaminated with S. typhimurium, making them free of bacterial contamination. Hens' eggs were artificially contaminated with S. typhimurium and subjected to various processes of cooking, frying and food preparation. It was observed that the minimum time necessary to eliminate contamination through cooking procedures is 5 minutes after the water starts boiling, and also that, cooking in the microwave oven complete eliminates the bacterial contamination. When the eggs were fried on both sides, keeping the yolk hard, a complete bacterial elimination was observed. Mayonnaise prepared with vinegar presented a decrease in bacterial colonies when compared mayonese prepared with lemon.

Keywords: Salmonella typhimurium; hen's eggs; mayonnaise; eggs cooked; eggs fried.

A salmonelose é uma grave doença de origem alimentar associada à presença de bactérias em ovos ou alimentos contendo ovos crus. No entanto, a utilização de procedimentos apropriados de cozimento e fritura pode eliminar esta contaminação. Há poucos estudos sobre a eliminação da contaminação de Salmonella em ovos de galinha por fritura em procedimentos típicos de cozinha, especialmente para Salmonella enterica serovar Typhimurium (S. typhimurium). O objetivo deste estudo foi verificar as condições apropriadas, para cozinhar e fritar ovos de galinha artificialmente contaminados por S. typhimurium, necessárias para torná-los livres de contaminação. Os ovos de galinha foram contaminados artificialmente por S. typhimurium e submetidos a vários processos de cozimento, fritura e preparação. Observou-se que o tempo mínimo necessário para eliminar a contaminação com o procedimento de cozimento é de 5 minutos após a fervura da água e que o cozimento no forno microondas eliminou a contaminação bacteriana. Com o procedimento de fritura, somente estão livres de contaminação os ovos fritos em ambos os lados mantendo a gema dura. Na preparação das maioneses, a maionese preparada com vinagre apresentou uma diminuição das colônias bacterianas quando comparada a maionese preparada com limão.

Palavras-chave: Salmonella typhimurium; ovos de galinha; maioneses; ovos cozidos; ovos fritos.

Salmonellosis is a foodborne disease caused by the consumption of contaminated food by Salmonella species (MEAD et al., 1999; SCHROEDER et al., 2005). Salmonella is a well-documented pathogen known to occur in a wide range of foods, especially poultry products (RIVOAL et al., 2009). The most incriminated foods are poultry meat and fresh eggs (OLIVEIRA; SILVA, 2000; PERESI et al., 1998). In most cases, the salmonellosis is caused by S. enteretidis contamination, but Salmonella enterica serovar Typhimurium (also known as S. typhimurium) can also provoke this disease (GUARD-PETTER, 2001). The enteric infections due to S. typhimurium and other Salmonella species develop gastrointestinal infection, with symptoms such as abdominal pain, diarrhea, low fever and vomiting (SHINOHARA et al., 2008).

Salmonellosis represents a significant cost to society in many countries and few countries report the data on economic cost of the disease. In the USA, there are estimates of 1.4 million non-typhoidal Salmonella infections resulting in 15,000 hospitalizations and 580 deaths annually. The total cost associated to Salmonella is estimated at US$ 3 billion annually in the United States (WORLD. 2009). 1,195 outbreaks of Salmonella were reported in Brazil in 2007, with 22.6% of them being provoked by the consumption of foods with raw eggs (CARMO, 2009).

Fresh eggs contamination by Salmonella species can be due to two possible mechanisms: contamination on the outer shell surface and internally. Internal contamination can be the result of penetration through the eggshell or by direct contamination of egg contents before oviposition, originating from infection of the reproductive organs. This is considered to be the major route of egg contamination and it should be controlled by applying sanitary measures at the breeders level (hygiene practices and eventually vaccination). External contamination can be reduced by preventing contacts between the laying hens and by cleaning and disinfecting the flock's environment (GANTOIS et al., 2009). Salmonella is known for its ability to asymptomatically infect the hen's oviduct (DE BUCK et al., 2004; NAMATA et al., 2004). It has not yet been clarified which route of contamination is the most important, but studies show that S. enteritidis is capable of penetrating the egg shell and subsequently reach the egg yolk (TODD, 1996; SCHOENI et al., 1995).

In Brazil, there are some reports confirming the presence of Salmonella species on the surface of egg shell and yolk, and in other food products commercially avaliable in markets (OLIVEIRA; SILVA, 2000; PERESI et al., 1998). The consumption of raw or slightly cooked eggs (in mousse, mayonnaise, beverages and other foods) contributes to an increase of the salmonellosis rate (RADFORD; BOARD, 1993; LOCK; BOARD, 1995), being necessary an incorporation of hygiene and disinfecting measures in the technology of fresh egg production (SCHOENI et al., 1995; MURCHIE et al., 2008). The risk of microbial contamination is minimal for hard-boiled eggs, but medium and certainly soft-boiled eggs are a potential risk factor for salmonellosis. The inactivation of S. enteritidis in eggs by boiling depends on the initial temperature of the egg. However, after 10 minutes of boiling, all S. enteritidis contamination is eliminated, independent of the initial temperature of the egg (GRIJSPEERDT; HERMAN, 2003).

Although there are many reports about the elimination of Salmonella contamination in eggs by boiling, there is a lack of studies on its elimination by frying and other types of cooking procedures, especially for S. typhimurium. Therefore, the aim of this study was to investigate the proper conditions to boil and fry S. typhimurium artificially contamined eggs and to evaluate the time of boiling and the frying procedure.

2 Materials and methods

Hens' eggs were obtained commercially and inspected. All the eggs with cracked shells or contaminated with feces were discarded. Prior the the experiments, the eggs were submerged in ethanol 70% (v/v) for 30 seconds and cleaned with a sterile towel to decrease the chance of external contamination (PERESI et al., 1998). Fifty eggs were selected and used to determine the average yolk weight (12.78 g) and also to confirm any prior Salmonella contamination as described in 2.3. Experimental work was started on the day the eggs were obtained and all procedures were carried out in room temperature.

2.2 Preparation of inoculum

A S. typhimurium (ATCC 14028) sample was grown overnight at 37 ºC in Salmonella-Shigella media (Himedia). After the incubation, some colonies of the culture were diluted in a sterile saline solution (NaCl 0.9%) up to 0.5 McFarland standard, to obtain a bacterial cell density around 10 8 CFU.mL -1 (OD₆₀₀ = 0.110) and diluted to 10 6 CFU.mL -1 . Then, 100 µL of the suspension (10 6 CFU.mL -1 ) was inoculated with a needle (25 × 48 mm) connected to 1 mL syringe into each egg at the 2 o'clock position in an approximately parallel path. The final bacterial concentration was approximately 10 4 CFU.g -1 of yolk (PERESI et al., 1998; NAMATA et al., 2004; MURCHIE et al., 2008). The position and size of the syringe was previously confirmed inoculating 100 µL of gentian violet, instead of the inoculum, in three eggs and breaking them into Petri dishes to visualize the presence of the dye in the yolk (COGAN et al., 2001). For each inoculation, the plunger of the syringe was drawn back to confirm that the needle had reached the yolk. Each hole was covered with quick-drying sterile adhesive, immediately after inoculation, to prevent external contamination. Eggs inoculated with the bacterial suspension were kept for 3 days at 25 ºC to promote the S. typhimurium growth and the subsequent yolk contamination.

2.3 Cooking eggs procedures

The artificially contaminated eggs were used in six cooking procedures in triplicates. Twelve them were cooked in a sterile becker with 200 mL of water for 0 (control), 3, 5 and 10 minutes after the water stared to boil. After the cooking, each egg was opened aseptically and the yolk was removed with a sterile spatula and transferred to a sterile Petri dish. The last 6 eggs were placed in sterile Petri-dishes. The eggs were aseptically broken and cooked in microwave oven for 40 or 60 seconds.

The verification of S. typhimurium contamination was carried out by removing a portion of the yolk, with the aid of bacteriological loop of one microliter, and inoculating it on Salmonella-Shigella media, being incubated for 24 hours at 37 ºC in a bacteriological incubator. After incubation, the presence of colonies was counted in a colony counter and expressed as log (CFU.mL -1 ).

2.4 Preparation of mayonnaise

Nine artificially contaminated eggs were used in three different mayonnaise preparations in triplicates. The eggs were broken aseptically and the raw yolks were transferred to a sterile becker. Around 100 mL of olive oil were added to the yolks and the mixtures were homogenized to get a creamy aspect. 2 mL of vinegar, lemon juice or water (control) were also added to the final mixture and homogenized again for at least 2 minutes. The verification of S. typhimurium contamination was carried out as described in 2.3.

2.5 Eggs frying procedures

Fifteen contaminated eggs were used in five frying procedures in triplicates. The contaminated eggs were broken aseptically and fried in a frying pan following procedures below: one side of the egg fried, keeping the yolk soft (procedure 1); both sides fried, keeping the yolk soft (procedure 2); one side of the egg fried, keeping the yolk hard (procedure 3); both sides fried, keeping the yolk hard (procedure 4); and not fried (as serve as control, procedure 5). The verification of S. typhimurium contamination was carried out as in 2.3.

2.6 Statistical analysis

Statistical analysis of the results was performed by variance analysis (ANOVA) completed with the post-hoc Tukey's test. For this, GraphPad Prism 5.0 (GraphPad Inc. San Diego, CA, USA) was used, accepting the level of significance of p

The elimination of S. typhimurium by cooking procedure in different times of boiling is shown on Figure 1. Before the cook procedure (0 minute), the contamination estimated in log (CFU.mL -1 ) was 6.51 ± 0.55. After 3 minutes the log (CFU.mL -1 ) downs to 3.12 ± 0.40, reaching zero after 5 minutes maintaining this condition up to 10 minutes. The curve fitted to observe the effect of the time of boiling on S. typhimurium growth show a r 2 = 0,92 and a half-life of 2.35 minutes. This result provided evidences of the efficiency of boiling water to eliminate the bacterial contamination when the cook procedure is realized at least for 5 minutes. The eggs cooked in microwave oven did not present any contamination [log (CFU.mL -1 )] = 0) showing a complete elimination of S. typhimurium under different times of cooking (40 or 60 seconds).

The frying eggs experiments demonstrate a worrying situation as seen in Table 1. The only procedure that was efficient to significantly eliminate S. typhimurium contamination was frying both sides of the egg keeping the hard yolk. All other procedures shows the presence of the bacterial contamination slighter then control but not significant different, except for procedure (1), where the bacterial growth is same as control.

The mayonnaise prepared with contaminated eggs shown a strong bacterial contamination confirming that the preparation of mayonnaise with raw eggs did not able to eliminate a further bacterial contamination (Table 2). When vinegar were added to the preparations, the contamination was slight reduced without statistical significance. The lemon juice did not have effect on S. typhymurium grown.

Foodborne diseases, such salmonellosis, are the biggest problem of international public health. In almost all cases, salmonellosis is caused by the consumption of foods containing raw or insufficiently cooked eggs (GUARD-PETTER, 2001; GANTOIS et al., 2009; PERESI et al., 1998; MURCHIE et al., 2008; MENSAH et al., 2002), which guarantees the persistence of contamination by Salmonella species. This contamination occurs even when there are low quantities of bacteria in yolk or albumen (HUMPHREY et al., 1991) and mild conditions of temperature, as evidenced by Grijspeerdt and Herman (2003), who reported that S. typhimurium growth was satisfactory at 25 ºC. This demonstrates the importance of storing eggs at lower temperature, at least at 4 ºC, what reduces the excessive growth of microorganisms (PERESI et al., 1998). However, low temperatures do not eliminate bacterial contamination, and the lack of suitable methods of food preparation as well as of material hygiene, may increase the risk of human contamination by Salmonella. Therefore, it is necessary to establish an appropriate cooking time in order to eliminate S. typhimurium in eggs. This study demonstrates that the contamination by S. typhimurium in eggs can be eliminated by cooking them for at least 5 minutes after the boiling water point (Figure 1). This result is close to those observed by Schoeni et al. (1995) using S. enteretidis, where the length of cooking observed for total elimination of bacterial contamination was of approximately 6 minutes after the water reached 100 ºC in bunsen burner. Inhibition of bacterial elimination of S. typhimurium in eggs when cooked in microwave oven confirmed the effect of microwave in the face of enterobacteria (PAPADOPOULOU et al., 1995).

The results of the mayonnaise preparations show the lack of efficiency of vinegar and lemon juice, which are normally added to mayonnaise in some countries, to eliminate the bacterial contamination. These procedures kept the food as a contamination vehicle, when prepared with raw eggs (ANDRADE; NEGRETE; OLIVEIRA, 2002).

The consumption of fried eggs could also lead to contamination by S. typhimurium if the procedure used for frying the egg is inadequate. This work tested several methods of frying eggs and some results were worrying, since the only procedure that was efficient to completely inhibit the bacterial growth was the one where the eggs were fried on both sides keeping the yolk hard. We observed the growth of S. typhimurium in all the eggs the yolk remained soft.. Even in the procedure where the egg was fried on one side and the yolk was kept hard, there was not a complete elimination of S. typhimurium contamination.

Initially, we believed that the condition of the yolk after the process of frying indicated the elimination of S. typhimurium in eggs. However, the results showed that this is not only the condition of yolk (soft or hard), that is an indicator of the elimination of bacterial growth, but also that the area of contact between the egg and the frying pan (fried on one side and fried on both sides) interferes on the process of bacterial elimination. It is believed that, in the procedure of frying the eggs on both sides until the yolk is hard, there is an increase in time and in the field of heat transfer between the frying pan and the egg, what could increase the efficiency of the removal of S. typhimurium, explaining why this procedure is more efficient than the other tested ones.

We concluded that, in order to have a complete inhibition of growth of the bacterium S. typhimurium possibly present in eggs or foods prepared with raw eggs, correct cooking and frying procedures are needed. The time required to eliminate S. typhimurium through the cooking procedure is of at least 5 minutes after the boiling of water, or to cook in microwave oven. Mayonnaise preparations with raw eggs are dangerous, because the bacterial contamination os still present even after the addition of vinegar or lemon juice. The fried eggs are safe from S. typhimurium contamination when they are fried on both sides keeping the yolk hard.

The authors would like to thank CNPq, FAPESC and UNESC for the financial support.

ANDRADE, J. Z.; NEGRETE, I. D. R. A.; OLIVEIRA, T. C. R. M. Evaluation of the cotamination by Staphylococcus aureus and Salmonella spp., of potato salad purchased at restaurants of Londrina, PR. Higiene alimentar, v, 16, p. 62-71, 2002. [ Links ]

CARMO,G. M. I. Vigilância Epidemiológica das Doenças Transmitidas por Alimentos no Brasil. Porto Alegre: ANVISA, 2008. Disponível em: . Acesso em: 24 jun. 2009. [ Links ]

DE BUCK, J. et al. Tubular glands of the isthmus are the predominant colonization site of Salmonella enteritidis in the upper oviduct of laying hens. Poultry Science, v. 83, p. 352-8, 2004. PMid:15049486. [ Links ]

MENSAH, P. et al. Street foods in Accra, Ghana: how safe are they? Bulletin of the World Health Organization, v. 80, p. 546-53, 2002. [ Links ]

PAPADOPOULOU, C. et al. Survival of enterobacteria in liquid cultures during microwave radiation and conventional heating. Microbiological Research, v. 150, p. 305-09, 1995. [ Links ]

SCHROEDER, C. M. et al. Estimate of illnesses from Salmonella enteritidis in eggs, United States, 2000. Emerging Infectious Diseases, v. 11, p. 113-5, 2005. [ Links ]

WORLD HEALTH ORGANIZATION - WHO. Drug-resistant Salmonella. 2005. Disponível em: . Acesso em: 24 jun. 2009. [ Links ]

Received 23/9/2009
Accepted 6/12/2009 (004423)

All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License

Posted October 25, 2018 at 4:15 PM ET

CDC, public health and regulatory officials in several states, and the U.S. Food and Drug Administration (FDA) External investigated a multistate outbreak of Salmonella Enteritidis infections linked to shell eggs from Gravel Ridge Farms.

• Reported Cases: 44
• States: 11
• Hospitalizations: 12
• Deaths: 0
• Recall: Yes

• On September 8, 2018, Gravel Ridge Farms recalled External cage-free large eggs with use by dates of July 25, 2018 through October 3, 2018 because they might be contaminated with Salmonella.
• Contact a healthcare provider if you think you got sick from eating recalled Gravel Ridge Farms shell eggs.
• Consumers and restaurants should always handle and cook eggs safely to avoid foodborne illness from raw eggs. It is important to handle and prepare all fresh eggs and egg products carefully.
  • Eggs should be cooked until both the yolk and white are firm. Scrambled eggs should not be runny. Egg dishes such as casseroles and quiches should be cooked to an internal temperature of 160°F or hotter.
  • Make sure that foods that contain raw or lightly cooked eggs, such as eggs over easy or hollandaise sauce, are made only with pasteurized eggs. Pasteurization kills disease-causing germs.
  • Wash hands and items that came into contact with raw eggs—including countertops, utensils, dishes, and cutting boards—with soap and water.

• As of October 25, 2018, this outbreak appears to be over.
• Forty-four people infected with the outbreak strain of Salmonella Enteritidis were reported from 11 states.
  • Illnesses started on dates ranging from May 17, 2018 to August 26, 2018.
  • Twelve people have been hospitalized. No deaths have been reported.
• Epidemiologic, traceback, and laboratory evidence indicated that shell eggs from Gravel Ridge Farms were the likely source of the outbreak.
• On September 8, 2018, Gravel Ridge Farms recalled cage-free large eggs with use by dates of July 25, 2018 through October 3, 2018 because they might have been contaminated with Salmonella.

• Most people infected with Salmonella develop diarrhea, fever, and stomach cramps 12 to 72 hours after being exposed to the bacteria.
• The illness usually lasts 4 to 7 days, and most people recover without treatment.
• In some people, the diarrhea may be so severe that the patient needs to be hospitalized. Salmonella infection may spread from the intestines to the bloodstream and then to other places in the body.
• Children younger than 5 years, adults older than 65 years, and people with weakened immune systems are more likely to have a severe illness.

CDC, public health and regulatory officials in several states, and the U.S. Food and Drug Administration (FDA) External investigated a multistate outbreak of Salmonella Enteritidis infections.

Public health investigators used the PulseNet system to identify illnesses that were part of this outbreak. PulseNet is the national subtyping network of public health and food regulatory agency laboratories coordinated by CDC. DNA fingerprinting was performed on Salmonella bacteria isolated from ill people by using techniques called pulsed-field gel electrophoresis (PFGE) and whole genome sequencing (WGS). CDC PulseNet manages a national database of these DNA fingerprints to identify possible outbreaks. WGS gives a more detailed DNA fingerprint than PFGE. WGS performed on bacteria isolated from ill people showed that they were closely related genetically. This means that people in this outbreak were more likely to share a common source of infection.

As of October 24, 2018, 44 people infected with the outbreak strain of Salmonella Enteritidis were reported from 11 states. A list of the states and the number of cases in each can be found on the Map of Reported Cases page.

Illnesses started on dates ranging from May 17, 2018 to August 26, 2018. Ill people ranged in age from one year to 94, with a median age of 32. Sixty percent of ill people were female. Of 37 people with information available, 12 (32%) were hospitalized. No deaths were reported.

WGS analysis did not predict antibiotic resistance in bacteria isolated from 25 ill people and 1 food sample. Testing of three clinical isolates using standard antibiotic susceptibility testing methods by CDC’s National Antimicrobial Resistance Monitoring System (NARMS) laboratory also did not show antibiotic resistance.

Epidemiologic, traceback, and laboratory evidence indicated that shell eggs from Gravel Ridge Farms were the likely source of this outbreak.

State and local health officials interviewed ill people and asked questions about the foods they ate and other exposures in the week before they became ill. Twenty-six (81%) of 32 people interviewed reported eating restaurant dishes made with eggs. This percentage was significantly higher than results from a survey Cdc-pdf [PDF – 787 KB] of healthy people in which 38% of respondents reported eating any eggs away from home in the week before they were interviewed. These restaurants reported using shell eggs in the dishes eaten by ill people.

FDA and state partners traced the source of the shell eggs supplied to these restaurants. Gravel Ridge Farms in Cullman, Alabama, supplied shell eggs to restaurants where 20 of the 26 ill people ate eggs. Several ill people lived in states where Gravel Ridge Farms shell eggs were not sold, but most traveled to states where they were sold in the week before their illness began.

The outbreak strain of Salmonella Enteritidis was identified in environmental samples from Gravel Ridge Farms. Officials in Alabama also collected eggs from the Gravel Ridge Farms facility for testing. The outbreak strain of Salmonella Enteritidis was identified in these eggs. WGS results showed that the Salmonella bacteria from the environmental samples and from Gravel Ridge Farms eggs were closely related genetically to the Salmonella bacteria isolated from ill people. These results provided more evidence that people in this outbreak got sick from eating shell eggs from Gravel Ridge Farms.

On September 8, 2018, Gravel Ridge Farms recalled External cage-free large eggs with use by dates of July 25, 2018 through October 3, 2018 because they might have been contaminated with Salmonella bacteria.

Eggs from small flocks of chickens are more likely to be contaminated with Salmonella enteritidis than eggs sold in grocery stores, which typically come from larger flocks that are regulated by the U.S. Food and Drug Administration, according to researchers in Penn State's College of Agricultural Sciences.

That conclusion -- which flies in the face of conventional wisdom that eggs from backyard poultry and small local enterprises are safer to eat than "commercially produced" eggs -- was drawn from a first-of-its kind, six-month study done last year in Pennsylvania. Researchers collected and tested more than 6,000 eggs from more than 200 selling points across the state.

Salmonella enteritidis is a leading foodborne pathogen in the United States, with many outbreaks in humans traced back to shell eggs. The FDA requires shell-egg producers from farms with more than 3,000 chickens be in compliance with the FDA Final Egg Rule, which is aimed at restricting the growth of pathogens. However, small flocks with fewer than 3,000 layer chickens currently are exempted. Eggs from these producers often are marketed via direct retail to restaurants, health-food stores and farmers markets, or sold at on-farm roadside stands.

From April to September 2015, the researchers purchased two to four dozen eggs from each of 240 randomly selected farmers markets or roadside stands representing small layer flocks in 67 counties of Pennsylvania. Internal contents of the eggs and egg shells were cultured separately for Salmonella using standard protocols. Salmonella recovered were classified by serotype, and any Salmonella enteritidis isolates present were further characterized to evaluate their relatedness to isolates of the bacteria that have caused foodborne illness outbreaks.

Test results revealed that of the 240 selling points included in the study, eggs from five -- 2 percent -- were positive for Salmonella enteritidis. Eggs sold at one of the positive selling points contained the bacteria in egg shells; the eggs from the other four selling points had Salmonella enteritidis in internal contents.

That is a higher prevalence of the pathogen than that found in studies of eggs from large flocks, noted lead researcher Subhashinie Kariyawasam, microbiology section head at Penn State's Animal Diagnostic Laboratory. Those eggs, from flocks of more than 3,000 birds, are subject to federal regulations aimed at reducing Salmonella enteritidis contamination.

These regulations require measures such as placement of Salmonella-"clean" chicks, intensive rodent control, cleaning and disinfecting between flocks, environmental monitoring of pullet and layer houses, continuous testing of eggs from any Salmonella-positive houses, and diverting eggs from Salmonella-positive houses for pasteurization.

Kariyawasam -- who presented the research findings to the American Veterinary Medical Association and the American Association of Avian Pathologists at their August meeting in San Antonio, Texas -- said the study clearly demonstrated that Salmonella enteritidis is present in the eggs produced by small flocks.

"The research highlights the potential risk posed by the consumption of eggs produced by backyard and small layer flocks. And, analysis of the Salmonella enteritidis present in the eggs from small flocks shows they are the same types commonly reported to the Centers for Disease Control and Prevention from human foodborne outbreaks," she said. "These findings emphasize the importance of small-producer education on Salmonella enteritidis control measures and perhaps implementation of egg quality-assurance practices to prevent contamination of eggs produced by backyard and other small layer flocks."

Eggs from small flocks make a negligible contribution to the table egg industry in the United States, Kariyawasam noted. But the growing demand for backyard eggs and eggs from nonfarm environments -- with small egg-producing flocks managed in cage-free systems and pasture situations -- suggests these production systems deserve some scrutiny.

"We were curious about Salmonella contamination of eggs produced by these flocks because the prevalence of this pathogen in smaller flocks was not known. Now we know that the prevalence of Salmonella enteritidis in eggs produced by small flocks is higher than in eggs produced by larger flocks."

Salmonella enteritidis, like other foodborne bacteria, is destroyed by proper cooking. However, Salmonella infections can be very serious, even life-threatening, especially to the very young, the elderly and people with weakened immune systems.

"The bottom line is, if you buy your eggs from the small producers, you need to worry about Salmonella just as if you bought eggs produced by large flocks," Kariyawasam said. "And, beyond the consumption of eggs, birds in these flocks can have Salmonella, so people with backyard poultry need to be aware of the dangers with pet birds -- there is a risk to allowing birds to come into the house and children playing with the chickens."