In the course of conducting inspections of egg farms, U.S. Food and Drug Administration personnel collect environmental samples in layer houses to look for the presence of Salmonella enteritidis and verify the efficacy of the farm’s Salmonella enteritidis prevention measures. According to industry sources, the FDA has also looked for other pathogens in some of the environmental samples. These sources report that when Salmonella Heidelberg was found in environmental samples, testing of eggs for Salmonella Heidelberg was required, and the farm was asked about control measures.
Dr. Richard Gast, U.S. Department of Agriculture Agricultural Research Service scientist, addressed the topic of Salmonella Heidelberg and eggs and their impact on human food safety at the United Egg Producers annual meeting in San Diego. He said that there isn’t a lot of research regarding Salmonella Heidelberg, but he summarized the information that is available because of interest from the industry and the concerns raised by the FDA (see sidebar: What the FDA says about Salmonella Heidelberg and egg farms).
Salmonellosis cases not declining
Any discussion of Salmonella control programs in poultry, whether meat birds or layers, needs to be viewed in light of the lack of progress in reducing the number of cases of human salmonellosis in the U.S., according to Gast. The incidence of human Salmonella infections in the U.S. did not decline between 1996-1998 and 2010, and the incidence of Salmonella enteritidis infections actually increased.
“Over 80 percent of human Salmonella enteritidis outbreaks with identifiable sources have been attributed to eggs,” Gast said. A USDA Food Safety Inspection Service risk assessment report estimated that 100,000 human illnesses may be caused annually in the U.S. by the consumption of shell eggs contaminated with Salmonella enteritidis. Gast stressed that the large Salmonella enteritidis outbreak in 2010 involving eggs, where 1,939 illnesses were traced to two Iowa egg producers and led to the recall of approximately 550 million eggs, has been a catalyst for heightened interest in eggs as a source of human illness.
Salmonella and poultry
Gast said that numerous Salmonella serotypes have been identified but that only a small proportion of these have ever been isolated from poultry; even fewer are common. A small number of serotypes account for most human salmonellosis, and many of the predominant human serotypes are similarly prevalent in poultry.
Laboratory confirmed human cases of salmonellosis reported to the CDC in 2009 had Salmonella Heidelberg as the fifth most common isolate, with 3.5 percent of the total cases (see Table 1). Over the last 40 years, Salmonella Heidelberg has consistently ranked in the top four or five of Salmonella serotypes from human sources, according to CDC data. In 1999 and 2002, Salmonella Heidelberg was the most common serotype of Salmonella reported to the USDA National Veterinary Services Laboratory (see Table 2).
Salmonella enteritidis, 17.5 percent, and Salmonella typhimurium, 15.0 percent, made up approximately a third of human illnesses according to CDC data for 2009. In third and fourth place in 2009 were serotypes Newport and Javiana with 9.3 and 4.9 percent, respectively.
Salmonella Heidelberg and human salmonellosis in the US
In 1986, there was a Salmonella Heidelberg outbreak in New Mexico, which affected 91 people; it was associated with the consumption of eggs at a convention breakfast. In a study of 44 sporadic illnesses due to Salmonella Heidelberg occurring in 1996-1997, eating eggs prepared outside of the home was the only significant risk factor reported (37 percent attribution).
In a study of 101 Salmonella Heidelberg outbreaks occurring in 1973-2001 with identifiable food vehicles, 25 percent were associated with poultry meat, 20 percent with eggs or foods containing eggs, and 8 percent with both poultry and eggs.
In 2004, frozen chicken nuggets and strips were associated with Salmonella Heidelberg infections in British Columbia. In 2011, ground turkey was implicated as the source of a Salmonella Heidelberg outbreak that affected 136 people in 34 states.
Salmonella Heidelberg and eggs
“Heidelberg is a highly prevalent serotype in poultry in general and in egg type flocks in particular,” Gast said. “But what does that mean?” He explained that the deposition of Salmonella in the egg is a consequence of the colonization of reproductive organs, particularly the ovary and upper oviduct, in systemically infected hens.
“If the ovary is infected, then it is likely that the Salmonella Heidelberg will end up in the yolk,” he said. “If the oviduct is infected, then it is more likely that the Salmonella will be in the albumin.” Researchers have been able to isolate Salmonella enteritidis, Salmonella Heidelberg and Salmonella typhimurium from the ovaries of naturally infected hens.
Gast said that, experimentally, if you give specific pathogen free, or SPF, hens very large (1 billion cells) oral doses of Salmonellas, including Salmonella Heidelberg, you can get Salmonella in the hen’s feces, tissues and eggs. Gast, who conducted some of this research in his laboratory, said that this is an unrealistically large dose that is used to get a result. “We should not infer from data obtained using these mega doses that this is the naturally occurring phenomenon,” he said. He also explained that it is easier to infect an SPF bird than it is to infect a bird raised in a commercial setting, and with a higher response, but this doesn’t necessarily reflect what would happen to commercial birds.
Salmonella enteritidis more dangerous than Salmonella Heidelberg
In inoculated day-old chicks, Salmonella Heidelberg isolates caused moderate mortality, similar to Salmonella enteritidis, but much lower than Salmonella pullorum and Salmonella typhimurium. Salmonella Heidelberg isolates were associated with lower frequencies of vaginal colonization and egg contamination after intravaginal inoculation, and reproductive organ colonization after intravenous inoculation, than Salmonella enteritidis isolates.
“In birds with infected internal organs, Heidelberg does get to the reproductive tissues at the same rate or maybe even a little higher than enteritidis does,” Gast said. This research was conducted with four strains of Salmonella Heidelberg and one of Salmonella enteritidis, and Gast questioned whether or not this is indicative of the other strains of Salmonella Heidelberg and Salmonella enteritidis that are in the environment. All four strains resulted in some birds that produced internally contaminated eggs, but at a lower rate than was found for Salmonella enteritidis. Only 1-4 percent of the Salmonella Heidelberg infected birds produced contaminated eggs versus 7 percent of the Salmonella enteritidis infected birds.
In all his work, Gast said that Salmonella Heidelberg infected hens do not produce contaminated eggs at anywhere near the rate at which Salmonella enteritidis infected hens produce contaminated eggs. He said that a dose of Salmonella Heidelberg that hens in the field might be exposed to would be around 10,000 cells, and at that dose, very few eggs would be contaminated. He said that Salmonella enteritidis is better at penetrating and growing in the yolk than Salmonella Heidelberg. Even though Salmonella enteritidis is better at getting in the egg than Salmonella Heidelberg, it still does so at a relatively low rate. Gast said that in the two major field studies of Salmonella enteritidis, one in California and the other in Pennsylvania, in flocks that are known to be in environmentally positive houses, only 0.25 percent of the eggs were positive for Salmonella enteritidis.
Preventing human salmonellosis
Gast said that there are both pre- and post-harvest control measures that can be taken to reduce the incidence of human salmonellosis. Pre-harvest controls should minimize opportunities for the introduction, persistence, and transmission of flock infections with Salmonella.
Post-harvest controls should safeguard the microbial integrity of food products or decontaminate them before consumption. Examples of post-harvest controls are egg washing, refrigeration, pasteurization and cooking. Inactivation of Salmonella Heidelberg by heating or cooking is similar to Salmonella enteritidis. The effects of refrigeration on Salmonella Heidelberg survival are similar to Salmonella typhimurium.
There are two types of pre-harvest control strategies, according to Gast: serotype-independent and serotype-specific. Serotype-independent controls are broadly directed against all serotypes, and in some instances, against other microorganisms as well. Sanitation, biosecurity and pest control programs are examples of serotype-independent controls, and these have broad cost effectiveness.
Serotype-specific controls are targeted to act with precision against particular serotypes with distinctive public health or economic significance. Testing and vaccination are the two prime examples of serotype-specific controls used by egg producers to prevent Salmonella enteritidis contamination of eggs.
Gast said that ELISA tests for other serogroup B Salmonella strains, such as inactivation of Salmonella Heidelberg by heating or cooking, is similar to Salmonella enteritidis. The effects of refrigeration on Salmonella Heidelberg survival are similar to Salmonella typhimurium, may also detect Salmonella Heidelberg. Probiotic cultures can be used to competitively exclude Salmonella from the digestive tract of poultry. Gast said that probiotic cultures are similarly effective against Salmonella Heidelberg as they are against other salmonellae.
There is no commercially available vaccine for layers against Salmonella Heidelberg at this time. Experimentally, bacterins containing Salmonella Heidelberg or other serogroup B Salmonella strains, such as Salmonella typhimurium, have reduced cecal colonization after Salmonella Heidelberg challenge. Vaccination of hens with an Salmonella Heidelberg bacterin offers some protection for the offspring of the vaccinated hens; this is not the case for Salmonella enteritidis.
“There will probably be considerable long term discussion about where we are going,” Gast said. “I am not going to tell you what we ought to do; that is policy.”
He said that questions have been posed in the past about what impact controlling or excluding one strain of Salmonella from poultry will have on other organisms in the birds. For instance, will controlling Salmonella enteritidis leave a niche open for another Salmonella serotype? He mentioned a paper written years ago, which asked if control of pullorum left a niche open for enteritidis. He asked that if in the future, as we eliminate one Salmonella serotype at a time, will we just create an opening for another organism? Will this give us an ever-expanding list of organisms that we are trying to control?