Spillover

by David Quammen

  And eventually did. Twenty more years passed before Rudolph J. Scrimenti, still another dermatologist, practicing in Milwaukee, had reason to recall Hellerstrom’s paper, which he had read as a medical student. Scrimenti, in 1970, became the first physician to report a case of erythema migrans in America. His patient, a fellow physician, had been bitten by a tick while grouse hunting in central Wisconsin, and the rash grew outward from the site of the bite, eventually encircling much of his chest, right armpit, and back. Scrimenti treated the symptoms with penicillin. In his brief published report, he echoed Hellerstrom’s guess that it might have been caused by a spirochete, but Scrimenti hadn’t been able to find one.

  This is all part of the medical groundwork that was available—though not conspicuously available—when doctors at the Yale School of Medicine heard about the cluster of juvenile arthritis cases in Lyme, Connecticut. One of those doctors was Allen C. Steere, a first-year fellow in the rheumatology division. Rheumatology is the science of joint disorders such as rheumatoid arthritis, which is an autoimmune condition, not an infectious disease. Juvenile rheumatoid arthritis, Steere recognized, should not be occurring in any such cluster. It didn’t pass from one patient to another. It didn’t infect people through their drinking water. It didn’t fly on the wind like Q fever . . . did it?

  Steere and his colleagues followed out the cases brought to their attention, did some further epidemiological legwork, found many more cases in roughly the same area, and began calling the syndrome “Lyme arthritis.” Steere’s group also took note of the associated symptom among a sizable fraction of the patients: a circular red rash. Other medical practitioners, in Connecticut and nearby parts of New York, also saw cases of this peculiar skin inflammation and began wondering. Was it caused by an insect bite? Was it the same condition, erythema migrans, that had been described in the literature from Europe? About that point, in the summer of 1976, a field biologist named Joe Dowhan, working in a forested area some miles east of Lyme, pulled a tick off his leg and dropped it into a jar. Dowhan had noticed the bite because, unlike most other tick attachments he’d experienced in his career, it registered as a small, painful nip. Three days later, he developed a rash. As the red circle grew, he remembered having seen an article about Allen Steere’s work. So he called, got an appointment, sat through an exam, and then handed Steere the tick.

  Dowhan’s specimen was identified as Ixodes scapularis, commonly known as the deer tick, an arthropod widely distributed throughout the eastern and midwestern United States. This became an important but ambiguous clue in the Lyme disease story, leading both toward insight and into confusion. The insight came first. Fieldwork along the lower Connecticut River revealed that Ixodes scapularis ticks were far more numerous in small woodlands and brush on the east bank of the river—the bank on which sat the village of Lyme—than on the west bank. That finding, combined with the fact that human cases also were far more common on the east bank, pointed further suspicion at the “deer tick” as a vector of what even Steere and his rheumatologist colleagues, having dropped the term “Lyme arthritis,” were now calling “Lyme disease.”

  The confusion grew more slowly. If the “deer tick” carried the pathogen (whatever it was) and infected people like Joe Dowhan by biting them, then the abundance of human cases must reflect the abundance of ticks, and the abundance of ticks must reflect the abundance of deer in those suburban woodlands of coastal Connecticut. Yes?

  No. This was an ecological system with the intricacy of chess, not a board game with the clarity of checkers, and its cause-and-effect relations weren’t nearly so simple. The “deer tick,” as later research has shown, lives a complicated life.

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  Willy Burgdorfer meanwhile made his crucial discovery of the pathogen itself, giving a name and a biological identity to the agent responsible for the mysterious clusters of cases.

  Burgdorfer was a Swiss-born and Swiss-trained microbiologist with a shovel-wide jaw, a cagey smile, a great domed head like Niels Bohr, and a deep interest in medical entomology. He did his doctorate on a tick-borne spirochete, Borrelia duttonii, which in Africa causes an illness called relapsing fever. By the time he finished that project, Burgdorfer had dissected thousands of ticks to scrutinize their innards. He had also invented a quick, practical technique for determining whether a given tick carries spirochetes: snip off a leg and look through a microscope at the body juice (hemolymph) that dribbles out. Emigrating to the United States, in 1952 he joined the Rocky Mountain Laboratory, in Hamilton, Montana, the same facility where Herald Cox and Gordon Davis had done their work on Q fever. In fact, Davis became his early sponsor there, and for a couple years Burgdorfer continued to work on Borrelia spirochetes (and the variants of relapsing fever they cause in America) among captive tick colonies that Davis had established. Some laboratory scientists work with fruit flies, some with carefully inbred mice; Davis and Burgdorfer nurtured teeming cagefuls of ticks.

  Then the winds changed: A high administrator told young Willy Burgdorfer that relapsing fever was “a disease of the past,” no longer justifying government-supported research, and advised him to pick a different specialty. By his own later account, Burgdorfer followed that advice only partially. He managed to stay at the Rocky Mountain Laboratory (which remained a leading research institution, despite its remote location), doing his primary work on plague, Rocky Mountain spotted fever, and other infamous diseases while pursuing his special interest in tick-borne spirochetes as “a moonlighting job.” When Gordon Davis retired, Burgdorfer inherited the elder man’s lab technician and his captive colonies of ticks. All of this qualified him well for the role he would eventually play with Lyme disease.

  Almost three decades later, near the end of his own career, Burgdorfer’s lifelong interest became urgently relevant. By the late 1970s, Allen Steere and others had begun to suspect that what they had first called “Lyme arthritis” was actually a tick-borne infectious disease, which had affected 512 patients, mostly along the northeastern seacoast and in Wisconsin. Hundreds more cases would soon be reported by the CDC. Around the same time, a family practitioner on Shelter Island, New York, just across the Long Island Sound from Lyme, was treating patients with similar histories—unusual feverish ailments that seemed to have been transmitted by ticks. Other tick-borne diseases also occurred on Shelter Island, a small but insalubrious place, so Lyme disease there was just one hypothesis among several. Then a batch of ticks, collected from low vegetation on Shelter Island, was sent out to Burgdorfer’s lab in Montana, where he dissected their gut cavities and found more than 60 percent of them harboring some sort of spirochete. “No longer did we hear, ‘get out of the spirochete business,’ ” Burgdorfer recalled later. Spirochetology was back in fashion. These ticks were alive with tiny corkscrewing forms.

  When Burgdorfer and his colleagues allowed infected ticks to feed on white laboratory rabbits, the rabbits developed circular skin rashes that grew outward like ripples from the bites, replicating the telltale annular pattern seen so often in human cases. Burgdorfer’s group also cultured the spirochete from ticks and then tested it against antibodies in blood sera from Lyme patients. The positive results in those tests, plus the rabbit reactions, constituted evidence that they had found the agent of Lyme disease. This was how Burgdorfer earned his place in what he later jovially called the “lymelight.” When other researchers wrote up a formal identification of the spirochete, shortly afterward, they named it Borrelia burgdorferi in his honor. The only hitch in this tale of elegant lab science is that the identity of the ticks was still a matter of confusion.

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  It was confused in two ways, one of which is more interesting for our purposes than the other. The uninteresting confusion involved the scientific name. Was it Ixodes scapularis carrying the Lyme spirochete in those coastal New England habitats, or did the creature belong to a similar but undescribed species, which should be given its own scientific identity? For a while the Lyme-bearing tick becam
e known as Ixodes dammini, until further taxonomic scrutiny invalidated that distinction, in 1993, and restored it to Ixodes scapularis. This back-and-forthing was merely a matter of taxonomic practice, reflecting the chronic tension between splitters (who like to delineate many species and subspecies) and lumpers (who prefer fewer). The splitters won a temporary victory; the lumpers prevailed.

  A second sort of confusion, more consequential, derived from uncertainty over the tick’s less formal label. As Ixodes scapularis, it had been familiarly known as the blacklegged tick. When it was mistakenly split off into a new species, it received also a new common (but not very common) name, “Dammin’s northeastern deer ixodid.” That clumsy phrase was later shortened to “deer tick.” Name-giving influences perception, of course, and “deer tick” reinforced a misunderstanding about the little beast in question: that this blood-sucking, disease-transmitting arthropod is somehow uniquely associated with deer. Wrong.

  Calling it the “deer tick” led to a mistake of circularity. If white-tailed deer are the host animals from which “deer ticks” draw their crucial sustenance, and “deer ticks” are the vectors that transmit Lyme disease to humans, it would seem to follow logically that high deer populations must contribute to high levels of human infection. It does follow logically—but erroneously. The syllogism would be sound, except that its first premise is oversimplified and misleading. “Deer ticks” of the species Ixodes scapularis do not draw their crucial sustenance from deer.

  An ecologist named Richard S. Ostfeld has done much to untangle this confusion. Ostfeld made a two-decade investigation of one ecosystem, in suburban New York, within which Borrelia burgdorferi lives. He also reviewed the research done elsewhere and the conclusions that had been (sometimes erroneously) drawn. White-tailed deer, he found, are a misleading distraction. Ostfeld’s book on the subject, Lyme Disease: The Ecology of a Complex System, appeared in 2011. “The notion that Lyme disease risk is closely tied to the abundance of deer arose from field studies that began shortly after the discoveries of the bacterial agent of Lyme disease and the involvement of ticks as vectors of these bacteria,” he wrote. Those studies were thorough and energetic, he noted, but perhaps driven too much by desire for a simple answer from which public health actions could be taken. Their context was “the hunt for the culprits—the critical species.” One journal article had called white-tailed deer “the definitive host” of the tick. According to another study, the deer was “the one indispensable piece” of the Lyme disease puzzle in North America. An overview account, otherwise excellent and written by a doctor with an acute sense of the medical issues, had pounced on the same conclusion as a way of explaining why Lyme seemed to be a newly emergent disease: “If the Lyme spirochete had been around for so long, why did it begin to surface as a recognized medical entity only in the past few decades? This question can be answered in one word—deer.” They all agreed: deer deer deer. The one-word answer seemed to point toward a pragmatic solution to the problem of Lyme disease: Reduce the number of infected ticks by reducing the number of white-tailed deer.

  And so that was tried. In one early effort, on a small island off Cape Cod, state wildlife biologists shot 70 percent of the deer; then researchers assessed the effect on tick populations by counting tiny, immature ticks on one kind of mouse. Result: The abundance of ticks on the mice was at least as high as before deer eradication. In years since, heavy deer-hunting has been encouraged in some areas of Maine, Massachusetts, Connecticut, and New Jersey for the sake of drawing down deer populations, while researchers again monitored the effects, if any, on populations of ticks. The town of Dover, Massachusetts, for instance, recently announced its first deer hunt on open town land, reflecting recommendations from the local board of health and the Lyme Disease Committee. Nineteen deer (sixteen does and three bucks) were killed, after which a Dover newspaper explained confidently: “The higher the number of deer in an area, the higher the chances are of spreading Lyme disease to humans.”

  Well, actually, no. That simple formula is as false as the notion that swamp vapors bring malaria.

  The premise behind such civic efforts is that the landscapes in question contain “too many” deer and that their overabundance accounts for the emergence of Lyme disease since 1975. And it’s true enough that there are lots of deer out there. Populations in the northeastern United States have rebounded robustly (because of forest regrowth, absence of big predators, lessened hunting by meat-hungry humans, and other factors) since the hard times of the eighteenth and nineteenth centuries. There might be more deer in Connecticut today than at the time of the Pequot War in 1637. But that abundance of whitetails, as Ostfeld’s work showed, is probably irrelevant to the chances you’ll catch Lyme disease during a stroll in, say, Cockaponset State Forest. Why?

  “Any infectious disease is inherently an ecological system,” Ostfeld wrote. And ecology is complicated.

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  Rick Ostfeld, seated in his office at the Cary Institute of Ecosystem Studies, in Millbrook, New York, his walls and door decorated with tick humor, told me that he’s a “heretic” on the subject of deer and Lyme disease. But he’s a heretic with data, not one who listens to private voices of revelation.

  Ostfeld is a fit, cheerful, fiftyish man with short brown hair and ovoid glasses. His primary research interest is small mammals. He studies the ways they interact, the factors affecting their distribution and abundance, the effects of their presence or absence, the things they carry. Since the early 1990s, he and his group at Cary have live-trapped tens of thousands of small mammals in the forest patches of Millbrook and neighboring areas—mainly mice, chipmunks, squirrels, and shrews, but also creatures as large as possums, skunks, and raccoons. Initially his research had nothing to do with Lyme; he was tracing population cycles of a native rodent, the white-footed mouse. Many kinds of small mammal tend to show such population cycles, passing from relative scarcity one year to abundance the next, even greater abundance the year after, and then crashing back to scarcity, as though governed by some mysterious rhythm. Many mammal ecologists have studied such cycles, trying to determine their causes. What drives the boom and the bust?

  Ostfeld was more curious about the consequences. When animal A becomes inordinately plentiful, how might that affect the populations of animals B, C, and D? Specifically, he wondered whether high population levels of white-footed mice might control outbreaks of a certain pestiferous moth by eating up most of the caterpillars. As he trapped his animals, examined them, and marked them with ear tags before release back into the understory, he noticed that their ears were covered with tiny dark bodies, as small as the dots of a colon: baby ticks. The mice were infested. They were supplying blood meals to the immature stages of Ixodes scapularis, known to Ostfeld as the blacklegged (not “deer”) tick. “Thus began my interest in Lyme disease ecology,” he wrote in the preface of his book.

  Over those twenty years, mammal by mammal, tick by tick, Ostfeld and his team collected an enormous body of information, and the work continues. They use Sherman live traps (from the H. B. Sherman company, of Tallahassee, a venerable supplier) baited with oats and set out on the forest floor. They release most of the captured animals alive, after a brief examination to check body condition and remove ticks. Small mammal biologists like him, for whom trap-and-release protocols are the daily routine of data gathering, tend to become highly adept—gentle but efficient—at handling live rodents. Ostfeld’s group has found that, in about one minute of close scrutiny, they can detect 90 percent of the ticks on a mouse. (They measured their own field-exam thoroughness by taking some mice into captivity after the one-minute check-over, holding them captive, and waiting for all ticks to fall off into a pan of water beneath the cage. Then they sorted the ticks from the mouse shit and other detritus—“a messy and challenging task,” Ostfeld testified—and counted this fuller total for comparison with what had been seen in the field.) For chipmunks, the method of quick visual inspection worked almost as w
ell. On other small mammals, including squirrels and shrews, the tick burdens were higher and harder to count, but Ostfeld’s group could still make well-informed estimates.

  Larval ticks are minuscule and even a tiny masked shrew, weighing only five grams (about the same as two dimes), carried on average fifty-five ticks, the researchers found. That’s a mighty burden of infestation for such a small, delicate creature. The short-tailed shrew, a larger animal, averaged sixty-three ticks per animal. Given Ostfeld’s estimate (also derived from trapping data) of about ten short-tailed shrews resident in an acre of woodland around Millbrook, it begins to add up to quite a few ticks, whole forests a-crawl with sanguineous dots, a disquieting prospect, even if the blacklegged tick never fed on anything but the blood of shrews.

  But it does. Its life cycle is complex. Like an insect, the blacklegged tick undergoes metamorphosis, passing through two immature stages (larva and nymph) on the way to adulthood. At each of those stages, it needs a single blood meal from a vertebrate host to nourish its transmogrification; an adult tick needs another blood meal to supply energy and protein for reproduction. In most cases the vertebrate host is a mammal, though it might also be a lizard, or a ground-nesting bird such as the veery, exposing itself to larval ticks on the forest floor. The blacklegged tick is such a generalist, in fact, that its menu of known hosts includes more than a hundred North American vertebrates, ranging from robins to cows, from squirrels to dogs, from skinks to skunks, from possums to people. “These ticks are unbelievably catholic in their tastes,” Ostfeld told me.