POKER PLAYERS’ PNEUMONIA
THREE OR four times a week, eight men and four women gathered for a few hours in the small room, playing poker, drinking beer, talking. From a social-health viewpoint, this group could be seen as exemplary: not only did it include members of both genders, but also some were of Caucasian and some of African heritage. They were clearly building a social support group (what the World Bank likes to call “social capital”), and there is good evidence that communities with a lot of social capital also tend to have better health.
That winter of 1987 in Halifax, Nova Scotia, the poker players didn’t pay much attention to the cat until Valentine’s Day, when she gave birth to three mewling kittens. That was pretty cool. One of the kittens died, but these things happen. That’s why cats have more than one in a litter and more than one litter in a lifetime. In so-called r/K selection theory, “r” strategists produce a lot of offspring and hope that some of them survive, and “K” strategists produce one or two and protect them with their lives; I would put cats slightly toward the “r” side (although not so far in that direction as, say, spiders).
On March 5, the cat’s owner got sick. Over the next couple of weeks the rest of the poker group came down with cough, chest pain, sore throat, nausea, vomiting, diarrhea, and, not surprisingly, fatigue. Eleven of them got better either spontaneously (perhaps because of the beneficial effects on the immune system of good social capital) or after medical treatment with antibiotics (which the World Bank might call human capital, and which we use when the social capital fails). One person, who had a heart problem to begin with, died. Joanne Langley, Thomas Marrie, and the other epidemiologists at Dalhousie University who investigated the outbreak and reported it in the New England Journal of Medicine dubbed it poker players’ pneumonia.
The disease that attacked the poker players is more widely known in the medical community as Q fever, a less interesting and less informative moniker. This is the kind of name given to a disease or agent when investigators don’t have a clue what they are dealing with; thus, aflatoxin poisoning in England was first called turkey-X disease, and the strain of hantavirus that laid low the Navajo in the Four Corners region of the American Southwest was called sin nombre (no-name). The name Q fever came from Australian physician Edward H. Derrick, who in 1935 investigated an outbreak of fever in abattoir workers in Brisbane, Queensland.
According to his colleague Macfarlane Burnet, who with David White later wrote the classic book The Natural History of Infectious Disease, Derrick rejected the name “abattoirs fever” because it might reflect poorly on the meat industry. He couldn’t use “X-disease” because it was already in use. Burnet suggested “Queensland rickettsial fever,” but this was rejected because it was considered derogatory to Queensland. Derrick finally settled on “Q” for “query” fever.
As part of his investigations, Derrick injected blood and urine from sick workers into guinea pigs, who, as stalwart pawns in the army against disease, also got sick. Unable to isolate any agent, Derrick took a saline emulsion of sick–guinea pig liver and sent it to Burnet in Melbourne. Burnet, later to win the 1960 Nobel Prize in Physiology or Medicine for his work in immunology, isolated the tiny organisms. They looked, he thought, a lot like rickettsiae, which are somewhere between bacteria and viruses in size and prefer the comfort of living inside cells to the rough-and-tumble life in the free world. If they were capable of thinking and writing, one might suggest they first penned the words later paraphrased by the poet Leonard Cohen, that the cell-free life might look like freedom, but it feels like death. If, as Lynn Margulis has suggested, we are, in whole or in part, communities of bacteria, Cohen’s lyrics take on a new layer of meaning.
At about the time Burnet was ferreting out the tiny organisms in Australia, Herald Cox and Gordon Davis at the Rocky Mountain Laboratory in Montana were studying ticks and the organisms they carried to try to understand two other zoonoses, Rocky Mountain spotted fever and tularemia, the latter a plague-like disease also called rabbit fever and deerfly fever, caused by a bacterium, Francisella tularensis, and transmitted to people through ticks, deerflies, or direct contact. A rare disease (about a hundred cases in the U.S. per year), tularemia is now considered a potential bio-terrorist agent, which to me indicates an unprecedented level of paranoia. Cox claimed to have cultivated rickettsiae from the ticks, but Dr. Rolla Dyer, director of the National Institutes of Health, was skeptical. Dyer visited Cox to challenge him and came down with fever, chills, sweats, and pain behind the eyeball (retro-orbital pain). In one of those rare instances where poetic justice does occur, blood from Dyer also made the guinea pigs sick. After the usual chaotic name calling that characterizes much microbial classification, investigators seem to have settled on the names Coxiella burnetii for the organism and coxiellosis for the disease (although “Q fever” is still widely used). Q fever is now reported from Uruguay to Portugal, from Russia to Australia, from Canada to China, from Switzerland to anywhere there are sheep and dust.
What was peculiar about the work of Thomas Marrie and his friends in Nova Scotia was that the disease was associated with cats. I have a paper in my files (somewhere) that reports quite definitively that cats do not get Q fever. I also have notes from veterinary school that say quite definitely that prions do not cross the species barrier, demonstrating not that such pronouncements prove science to be a bad thing but that science does progress and that scientists should be circumspect in their pronouncements. In this way, however, scientists are at a disadvantage against the pope, archbishops, grand ayatollahs, rabbinical teachers, evangelist preachers, and the presidents and prime ministers of many countries, who appear to have all the final answers.
Marrie went on to investigate the disease in the Maritimes and to review what is known globally about this zoonotic condition. He discovered that about 20 percent of community-acquired pneumonia in rural Nova Scotia was related to cat exposure, but he also investigated an outbreak related to skinning (dead, of course) wild rabbits. According to his team, almost half the snowshoe hares in the region had antibodies to Coxiella burnetii. One might suggest “wild-rabbit-skinning disease” as a good name, so as not to unfairly denigrate poker players or cats, but “Q fever,” being shorter and more neutral, may be less open to the political vagaries of public language.
Sheep and goats are considered the most common reservoirs for C. burnetii, and in a study our group did in Ontario in the late 1980s, we found that pretty well all flocks had some evidence of infection. Outbreaks and “abortion storms” associated with coxiella infection continue to occur in sheep and goat flocks around the world, but most animals carry the microbe without showing signs of illness.
This cryptic infection has been known for decades, and it was with some dismay and bemusement that I read reports that sheep were being taken into the Hospital for Sick Children in Toronto in the early 1980s, to be used for research. The sheep were dropped off in the basement of the nurses’ residence, then carted through a tunnel into the hospital itself and taken up to the ninth floor in an elevator also used by patients, visitors, and staff. As many as twenty sheep and a few goats were up there at any given time. If the research animals needed surgery, they were taken down to the eighth floor and sometimes walked down the hall. Nobody had reported getting sick, but an investigation found at least a dozen people who had had some variation of fever, diarrhea, coughing, muscle pain, and in one case hepatitis, that could be attributed to infection with Coxiella. The researchers almost seemed surprised.
Not long afterward, I phoned around to medical schools in southern Ontario to find out what kinds of courses were being offered on the epidemiology of zoonoses. Several thought such a course might be a good idea and had never heard of one that had been offered at Guelph for twenty years; diseases from animals were way off the medical radar.
Not long after the investigation at SickKids, and at about the time an outbreak in people who had contact with sick goats at the Royal Agricultural Winter Fair in Toronto was unfolding, one of the few veterinarians in the Ontario Ministry of Health was accosted by a new, perplexed minister of health with the question: what’s a veterinarian doing in the Ministry of Health? What indeed.
The late 1980s were a time of generally heightened concern (sometimes verging on panic) about Q fever and sheep. The incidents at Toronto SickKids and community outbreaks stimulated a review of how sheep are screened before entering research centers in Canada, including the Ontario Veterinary College, where I worked. Veterinary students learn a lot of important things from sheep, although not how to panic and run at unexpected noises, which is a good thing for future clients. For four years, in parallel with the procedural changes for disease-screening experimental sheep, I ran a “blood-for-doughnuts” program. In return for doughnuts and coffee, students in one veterinary class donated blood every semester and filled in little questionnaires about exposure to animals. I followed the class from their first year all the way through to graduation, but only one or two of them showed any evidence of exposure, and that wasn’t at the vet college. One could almost hear an administrative sigh of relief.
But sheep and goats aren’t the only reservoirs, as Thomas Marrie demonstrated. One of my late colleagues in Ontario, Gerhard Lang, who himself suffered from a chronic form of Q fever, found widespread evidence of exposure to the agent in cattle as well. There is evidence that infected cattle can shed it in their milk for more than two years, but, although the cattle in Ontario had antibodies, indicating that they had been exposed, there was no evidence that they were actively infected.
Researchers and veterinarians don’t have a very good idea which animals might be carrying and shedding the organism; it is very infectious at small doses (one organism is apparently enough to make a person sick), and laboratory technicians are not keen to work with it. We are therefore left with secondary evidence, such as antibodies in serum, which indicate that the animals were once exposed to the organisms but don’t say much about current infection or shedding.
In the absence of abortions and stillbirths in animals, there is not much to go on, either in animals or people. Clinical signs (things that can be seen and measured, such as temperature) and symptoms (things that are felt, such as pain and headaches) aren’t unique to Q fever. The disease also varies from place to place, probably depending on particular strains of the organism. In the Maritimes of Canada, pneumonia seems to be the main disease; in other places, it is hepatitis, diarrhea, or general “flu-like” syndromes, which is why it is not surprising that the hospital-infection-control people in Toronto had not detected an outbreak until after it had occurred. Chronically, Coxiella can stick to heart valves and cause a debilitating endocarditis.
I have left one question hanging in the air: how do people get the disease from animals? In the summer of 1981, twenty-nine people in Gwent, south Wales, came down with fever, severe headaches, and malaise. “Malaise” is a technical term for feeling bummed out, under the weather. (I sometimes ponder, as a specialist in zoonoses, what wonderful afflictions I might be suffering. Alas, I suspect my malaise has more to do with newspaper headlines than bacteria, viruses, or rickettsia.) Two of those afflicted in Gwent county developed something considerably more serious than my middle-class, hypochondriac whinging: hepatitis and endocarditis. The person with the infected valves died, and the cause of death was demonstrated by infecting and then sacrificing a guinea pig; those who say animal sacrifice is obsolete little know the costs of our well-being and scientific knowledge. Investigators followed every possible lead as to how people got infected. In the end, they decided that farm trucks had driven through the neighborhood, stirring up clouds of contaminated straw and manure.
At least the good people in the villages of Val de Bagnes in Valais Canton, Switzerland, enjoyed the pleasures of watching sheep, and not just ramshackle trucks, flock down their valley from mountain pastures to market. The autumn of 1983 was an especially dry one, and over four hundred villagers came down with Q fever. About half the people had shivering, severe headaches, severe exhaustion, and loss of appetite. Some of them had more severe chest pains, coughs, dizziness, and abdominal pains.
According to the investigators, “More than half of the patients suffering from Q fever were not seen by a doctor, being either only slightly ill or not ill at all.” This is an interesting use of the word “suffering,” which I shall have to keep in mind when tallying up a lifetime of such afflictions. On the plus side, the researchers made the remarkable suggestion that physicians and veterinarians talk to each other and perhaps even work together. After decades of resistance, diseases such as Q fever, avian influenza, and West Nile virus have encouraged some movement in that direction.
What almost all the outbreaks have in common is that fluids and materials from animals that have recently given birth spill into the environment, dry up, and get blown around by the wind. They are tough and can survive a long time under difficult environmental conditions. Near Aix-en-Provence, France, investigators attributed higher rates of the disease to a local wind, the mistral, which came down from the northwest and passed over a sheep-rearing area before entering the small town of Martigues; the pristine air of southern France was harboring more than romance for starry-eyed tourists. Some cases have been traced to drinking infected milk, but I suspect that the milk splashed and people breathed in the fresh, warm, down-home scent of infection. One version of the infection cycle shows Coxiella burnetii being transmitted from wild animals to people and domestic animals by ticks, which, given all the other bad stuff ticks carry, should not be surprising.
In 1978, four employees of an “exotic bird and reptile importing company” in New York State were set back with the usual fever, chills, and severe headaches. They had been unpacking and deticking a shipment of five hundred ball pythons (Python regius); the ticks were carrying Coxiella burnetii. Carriage by ticks is not thought to be common, but then who would have thought pythons were pets? The people who shipped the snakes from some tropical country must have shaken their heads in wonder; maybe they thought Americans eat them? The traffic in such so-called exotic pets is one of the most efficient ways for strange diseases to travel the globe.
In Poland, epidemiological patterns and experiments in mice suggested the possibility of sexual transmission, which could lead to all manner of inappropriate jokes. But I suppose a great many infections can be spread that way, depending on how one defines “sex.”
Many of us studying zoonotic diseases had begun to relegate Q fever to that “mostly of academic interest category” when, between 2007 and 2010, 4,026 human cases were reported from the Netherlands. Responses in the Netherlands involved culling tens of thousands of sheep and goats from flocks that tested positive, prohibition of breeding of sheep and goats, compulsory vaccination, and public education. There was a shortage of vaccine, however, and the vaccination program could not be fully implemented. Prohibition of breeding small ruminants was a major hardship for those whose livelihoods was based on selling sheep and goat milk. In February 2010, the Ministry of Agriculture, Nature and Food Quality in the Netherlands, together with the European Food Safety Authority and the European Centre for Disease Prevention and Control, hosted a conference titled “One Health in relation to Q-fever, in humans and animals.” The conference, which brought together experts from countries around the world, was remarkable in its holistic orientation, involving people from a variety of disciplines and jurisdictions, trying to pull together the best available global knowledge. Nevertheless, the absence of ecologists and environmental scientists, reflecting as it did the common practice of marginalizing natural scientists and ecologists from health management, made it a missed opportunity for advancing our understanding of the complex links between social and natural ecology—and helping us to get at some of the roots of the twenty-first-century “epidemics of epidemics.”