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Questions Abound in Q-Fever Explosion in the Netherlands

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Science  15 Jan 2010:
Vol. 327, Issue 5963, pp. 266-267
DOI: 10.1126/science.327.5963.266-a

A burgeoning goat-farm sector appears to be behind the worst outbreak ever recorded in humans of a rare zoonosis that until now has been seen primarily as a rare occupational disease for farmers, veterinarians, and slaughterhouse workers and as a potential—if not very deadly—bioterror agent.

VINKEL, NETHERLANDS—Jan van Lokven has been a goat farmer for 23 years, but he's about to lose half his livelihood. Later this month, government officials will show up at his barn to kill all of his pregnant goats—more than 60% of his flock of almost 650 animals. Drinking coffee at his kitchen table, Van Lokven says he isn't sure what he'll do that day. His animals would be more at ease if he's around while the culling team does its grisly job, he says. “I just don't know if I can watch it.”

Grisly job.

A vet injects marked, pregnant goats with a sedative during a mass culling operation at a Dutch farm.

CREDIT: MICHAEL KOOREN/REUTERS/LANDOV

Just before Christmas, the Dutch government decided to cull about 40,000 pregnant goats at more than 60 farms in hopes of halting the worst outbreak ever of a little-known bacterial disease called Q fever. The problem isn't that the goats are suffering; it's that they are microbiological time bombs that threaten human health.

Q fever causes little disease in animals, and most farmers don't see it as a problem. But it can lead to abortions and stillbirths—and when it does, the animals' placentas and birth fluids contain many billions of microbes that spread easily into the environment. Such outbursts are assumed to have caused increasingly bigger waves of human Q-fever victims—most of whom come down with pneumonia—in the Netherlands the past 3 years. In 2009, there were more than 2300 human cases, including six deaths.

Until now, Q fever has been seen primarily as a rare occupational disease for farmers, veterinarians, and slaughterhouse workers and as a potential—if not very deadly—bioterror agent. Nobody is sure what triggered the explosive outbreak in the Netherlands, which has sickened mainly people who never had contact with animals, so the small cadre of Q-fever experts elsewhere in the world are following the Dutch struggle with fascination. “Nothing like this has ever been reported,” says Jennifer McQuiston of the U.S. Centers for Disease Control and Prevention in Atlanta. She adds that between 100 and 170 human cases are reported annually in the United States. Faced with major gaps in scientific understanding and criticism that public health has taken a back seat to farmers' interests, the Dutch government has launched a flurry of studies of the disease and of Coxiella burnetii, the intracellular bacterium that causes it.

Q fever was first described in abattoir workers in Brisbane, Australia, in 1935. Its name—short for “query” because of its mysterious nature—was meant to be temporary, but it stuck even after C. burnetii was isolated in 1937. As it turned out, the microbe can be found almost anywhere in the world, and it has a bewildering range of hosts and ways to spread. It can infect mammals, birds, and arthropods, including ticks, which contribute to its spread by producing large amounts of it in their feces.

Scientists don't understand exactly why C. burnetii amasses in the wombs of pregnant animals, but past epidemiological studies have shown that the resulting abortions—especially in sheep and goats—are by far the biggest risk factor for human infections. However, human transmission from consuming contaminated milk and cheese, getting bitten by ticks, and having sex with an infected person have been reported as well.

In the United States, Q fever is classified as a “Category B” bioterrorism agent because it would be relatively easy to use and because, although not as deadly as anthrax or plague, attacks could still create widespread disease and panic. The U.S. Army exposed human volunteers to it as part of its biowarfare program in the 1950s; the Soviet Union experimented with it as well, as did the Japanese cult Aum Shinrikyo, known for its 1995 sarin attack. Bioterror worries brought more attention to it in the '90s and prompted the United States to make it reportable in 1999.

Rising tide.

The number of human Q-fever cases exploded in the past 3 years, and the disease, originally concentrated in the south, spread north and east.

SOURCES (LEFT TO RIGHT): RIVM/CIB/EPI; RIVM/CBS/VWA

This increased awareness—along with better diagnostic tests—may explain the rising number of reported outbreaks of Q fever over the past 10 years worldwide, says epidemiologist Didier Raoult of the Université de la Méditeranée in Marseille, France, the foremost expert in human Q fever. “Once you start looking for Q fever, you'll find more and more of it,” he says.

But what's going on in the Netherlands now is not just better detection but something new and different, says epidemiologist Roel Coutinho, head of the Centre for Infectious Disease Control in Bilthoven. When 182 human cases were detected in and around a town called Herpen in the summer of 2007, it seemed like a one-off outbreak. But in 2008, a new wave erupted, quickly filling up intensive-care units in the province of Noord-Brabant. A thousand cases were reported that year. In 2009, the number of new cases jumped to almost 2200, and the disease was found across the country.

It's still unclear what's behind the massive spread. Part of the reason has to be the recent expansion of high-intensity goat farming in the densely populated country, says Coutinho. The number of goats has quadrupled in Holland to more then 350,000 since 1995, and the number of them per farm has tripled; the country is now home to some of the biggest goat farms in the world. (In a sad twist of fate, some farmers switched to goats after a devastating swine flu outbreak ruined the Dutch pig industry in the 1990s.) Farms are often close together, and animals are frequently transported between them, presumably facilitating spread, says Coutinho. Bacteria released during abortions end up in manure, which is often spread onto farm fields; the wind may have carried them to the many surrounding towns and cities.

But Hendrik-Jan Roest, a scientist at the Central Veterinary Institute of Wageningen UR in Lelystad, says the sudden increase could be linked to a more virulent subtype of the microbe that started spreading in about 2005. Genetic typing by Corné Klaassen at Canisius Wilhelmina Hospital in Nijmegen has shown that all Dutch farms and patients are infected by a single subtype of C. burnetii. That suggests that the strain is somehow better at propagating itself than others, Roest says. He plans to compare strains in a collaborative study with Annie Rodolakis of the French National Institute for Agricultural Research in Tours, who has developed a mouse model of Q fever.

A more urgent question is how to bring the outbreak under control. In 2008, veterinary and public health authorities hoped that hygienic measures, such as a ban on distributing manure on farm fields, would help reduce human exposure. Now, the hope is that an animal vaccine produced by CEVA, a French company, can help bring the microbe under control. In short supply in 2008 and '09, the vaccine will be plentiful this year, says Christianne Bruschke, chief veterinary officer at the agriculture ministry. The vaccine does not prevent all infections, but it does prevent most abortions, which should help curtail the spread of the disease.

The vaccine does not work in infected animals, however, which is why an expert panel recommended in early December the emergency slaughter of all pregnant goats at affected farms. (There is no reliable way to quickly distinguish infected goats from healthy goats.) Bruschke says the cull is a one-time measure to prevent another massive release of microbes in the spring of 2010, when the goats would normally give birth. Then from 2011 on, the effects of the vaccine should start kicking in.

The impact on some farmers could be devastating, says Van Lokven. The Dutch government reimburses farmers for the current value of the goats but doesn't do so for the loss of income while they rebuild their flocks.

How well the measure will work is unclear as well. The huge numbers of C. burnetii already in the environment may persist for months or years; there's no good way to measure their numbers or to assess the threat they pose, says Roest. And there are many other questions. Although there is little doubt that goat farms are key amplifiers in the current outbreak, the role of cattle farms is unclear. For now, most experts say another surge of human cases this spring is inevitable—they just hope it will be smaller than that of 2009.

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