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Egg-loving salmonella bacteria have been sickening people for decades

By David Brown
Tuesday, September 14, 2010; HE01

The unfolding story of how salmonella bacteria infected two giant egg operations in Iowa this summer is the latest chapter of a mysterious narrative about how a minor bacterial annoyance took off 35 years ago to become the second most common cause of food-borne illness in the United States.

Like the things that cause AIDS, Lyme disease, Legionnaire's disease and West Nile fever, the egg-loving germ (whose formal name is Salmonella enterica serovar Enteritidis) is a classic "emerging infectious agent." Sometimes called SE, it's a microbe that has been around a long time and has found a new or better way to reach its human victims.

For more than three decades, the strain of salmonella bacteria with a fondness for eggs has taken advantage of changes in this country's animal husbandry, food distribution and eating habits.

Along the way, scientists and public health officials have paid increasing attention to it, culminating recently in the Food and Drug Administration's 71-page "egg safety rule," which took effect in July. The federal government hopes those regulations will prevent 80,000 of the 142,000 cases of egg-related salmonella infection that occur in the United States each year (out of an estimated 1.54 million cases of food-borne salmonella illness). They hope the rule will cut the number of infected "table eggs," currently estimated at 2.3 million of the 47 billion produced each year. The new standards might even reduce health-care costs by $1.4 billion.

But they are unlikely to eradicate the problem.

The problems in Iowa hark back to the early days of the SE pandemic. (The bacterium's worldwide, near simultaneous resurgence starting about 1980 has earned that designation.) Since April, health departments in 10 states have investigated 29 outbreaks of salmonella illness, all of them traceable to restaurants. Fifteen appear to be linked to eggs from a group of Iowa farms known as Wright County Egg, and at least one to a nearby operation, Hillandale Farms. In all, about 1,500 people have gotten sick. Such large, geographically dispersed outbreaks traceable to a single source are rare these days.

"This current outbreak is like deja vu," said Christopher R. Braden, the epidemiologist at the Centers for Disease Control and Prevention who is leading the Iowa investigation.

There are many species of salmonella bacteria, the most dangerous being Salmonella typhi, which causes typhoid fever, a frequently fatal bloodstream infection. One of the species that causes intestinal infection is Salmonella enterica, which has 2,500 distinct types, or serovars, all causing pretty much the same symptoms: vomiting, stomach pain, diarrhea and fever.

One of those serovars, SE, behaves differently from the others in crucial ways. In hindsight it's clear that something happened in the 1970s to break out it out of the pack.

From the mid-1970s to the mid-1980s, SE infections increased sixfold in the northeastern United States. In 1986, a large outbreak in New England that was linked to stuffed pasta shells gave epidemiologists two crucial insights: All the illness was egg-related and traceable to a single source, a farm in Connecticut that provided the eggs used in the stuffing.

For a while the SE problem was confined to the Northeast, where human cases peaked in 1989. Then it surfaced dramatically in California. It has slowly spread to the rest of the country, although it has always been rare in the Southeast for reasons unknown.

Not so perfect

As it happens, this wasn't SE's first appearance in eggs.

In the 1920s and 1930s, there was so much intestinal illness associated with duck eggs that that food -- once more popular than chicken eggs -- disappeared from the American table. There is good evidence that SE was the germ, one that would remain a low-grade threat for decades to come.

The discovery in the 1960s that the strains found in egg-associated outbreaks were the same ones found in the feces of the hens that laid the eggs led to rules requiring most eggs to be washed and inspected for cracks before they were sold. That caused a noticeable decline in egg-associated outbreaks, and by 1976 SE was responsible for only 5 percent of illness caused by all salmonella bacteria.

The reemergence of SE in the 1980s led to the search for other causes of illness, because eggs with dirty shells clearly weren't the explanation. It turns out the problem was "vertical transmission": passage of the microbe from mother to offspring, or, in this case, mother to egg.

In experiments done in the late 1990s and early 2000s at the U.S. Department of Agriculture, Richard Gast proved that SE-infected chickens could lay infected eggs.

When a hen eats something contaminated with SE, the bacterium can move from the intestine to the bloodstream and from there to the reproductive tract. If an ovary becomes infected, bacteria are often deposited in the yolk. If the oviduct, downstream from the ovary, is infected, the microbe is more likely to end up in the white. If the eggs were fertile, the resulting chicks may be infected. The hens often recover, and even when they are infected many of their eggs are entirely normal.

Nevertheless, news that nature's perfect food packages were sometimes disease-carrying grenades did not go over well.

"I think it would be fair to say that a lot of people on the industry side said that was not a viable theory," said Braden.

But the discovery should not have been a surprise.

Voluntary measures

The early-20th-century outbreaks of salmonella that ravaged chicken flocks, killing nearly 80 percent of newly hatched chicks, led to the creation of the National Poultry Improvement Plan in 1935. It advised farmers how to eradicate the bacteria and certify their flocks as disease-free. The NPIP was so successful that the serovar responsible for "fowl typhoid," Salmonella gallinarum, essentially disappeared.

Biologists later discovered that that bacterium's cell wall has a molecular feature, called the O antigen, identical to one in SE cells. They theorize that birds infected with S. gallinarum were immune to SE, which was more commonly carried by rodents. (A single mouse dropping can contain 100,000 salmonella cells.) When S. gallinarum disappeared, SE moved into its territory -- chickens.

From 1985 through 2003, 997 outbreaks of food-borne illness caused by SE were reported to health authorities. Three-quarters of the outbreaks involved eggs. The number of foods involved was extremely varied: ice cream, salad dressing, eggnog, omelets, crab cakes, chiles rellenos, pasta dishes, cream pies.

In all 33,687 people fell ill, and 82 died. However, that was just the tip of the iceberg; the CDC estimates that for every reported illness there are 38 unreported ones.

Those alarming numbers led some states to create voluntary "egg quality assurance programs" (EQAP) in which egg farmers instituted "biosecurity" practices, rodent-proofed their barns, routinely cultured henhouses for salmonella, tested eggs if the samples were positive, and followed specific disinfection procedures. Pennsylvania's program, started in 1994, is the model for the FDA rules that became mandatory nationwide this summer.

The programs made a big difference. A study published in 2004 showed that states with EQAPs experienced an average 72 percent fall in SE incidence in the 1990s. (Iowa, which produces more eggs than any other state and is the site of the recent problems, notably did not have an EQAP.) But since 2000 that decline has plateaued.

What happened?

Changes in bacterial or viral genes sometimes play a role in emerging infections. But, as often happens, factors beyond the microbe have contributed to the rise of the bug that is making consumers queasy.

"There are usually changes in the environment that permit rapid spread of an organism, where previously there wasn't an open door," said J. Glenn Morris, a physician who heads the Emerging Pathogens Institute at the University of Florida in Gainesville.

Industrial farming put huge numbers of birds in confined spaces heavily contaminated with their manure, which can harbor salmonella for as long as two years. Many farmers bought chicks from large suppliers, spreading the bacteria between regions. Some chicken farmers forced their hens to molt by starving them for a brief period. That dramatically increases the length of a hen's egg-laying life, but the stress can increase a bird's susceptibility to SE infection and increase the likelihood it will produce infected eggs.

At the same time, restaurants and food processors often pooled hundreds or thousands of eggs in cooking, allowing a few infected eggs to contaminate many dishes.

The "infectious dose" of SE isn't known, although some outbreaks suggest that fewer than 50 cells of the bacterium can make a person ill. The best way to avoid infection is to cook eggs until both white and yolk are hard, and to cook dishes containing eggs until the internal temperature reaches 160 degrees.

But what caused the U.S. pandemic to break out in New England in the late 1970s? And why did SE's prevalence increase simultaneously in South America and Europe? Was it the cumulative effect of these variables, or did something else happen? Did the bacterium become more virulent or American chickens more susceptible?

"That's the $64,000 question," said Robert V. Tauxe, a CDC scientist who has spent more than two decades studying food-borne infections.

The USDA's Gast agrees. "It's hard for me to believe that this just suddenly happened," he said recently. "It's very hard to explain under any of the scenarios."

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