Unfathomable? A team of scientists that mapped Borrelia burgdorferi’s genome in 1997 found an organism unlike any other disease-causing pathogen known to science. For one, it had “few, if any, recognizable genes involved in virulence,” the researchers wrote, while lacking the mechanics to make the basic building blocks of life. It simply takes what it needs, “apparently scavenging these necessities from the host,” they said. At the time, other scientists, writing in the journal Nature, said B. burgdorferi’s newly unveiled genome “challenged ideas of what a bacterial chromosome is,” with “an almost bewildering array” of genes unique among bacteria. More perplexing, it had qualities that suggested it could change its genetic signature—“to duplicate genes and rearrange them without much cost or damage.” Left unexplained, but perhaps hinted at, was why the organism could survive in so many places—from the salivary glands of ticks, to the joints of horses and mice, to the hearts and minds of humans—and, moreover, how it could persist in and migrate throughout its hosts. Those findings would come later.
To be sure, even after deer herds plummeted to near zero by 1900 and forests were clear-cut, Borrelia burgdorferi remained, unnamed, misunderstood, infecting ticks and people randomly. It was building slowly, in Europe in particular. Arvid Afzelius was perhaps the first physician to describe the Lyme rash, at a dermatology meeting in 1909 in Stockholm, Sweden, a country from which many future cases would come. A year later, a Viennese doctor reported three more rashes, and in 1911, a Swiss physician noted another. In 1913, an Austrian dermatologist and virologist Benjamin Lipschütz christened the radiating red mark “erythema chronicum migrans.” Over the next two decades more Lyme-like cases were reported, some with serious symptoms of paralysis, meningitis, and arthritic pain, many involving children, and all in Europe. In 1922, a fifty-eight-year-old sheep farmer in France was bitten by a tick on his left buttock, developed a plum-sized red rash, and is considered the first case of Lyme radiculoneuritis, which affects the nerve roots and causes numbness, tingling, and stabbing pain. According to the 2012 book “Aspects of Lyme Borreliosis,” Lyme disease was presumed in reports of children with colorful, radiating rashes in 1915 and 1920; in a thirty-four-year-old man with severe pain and fatigue in 1934; in twenty-three patients with facial palsy, severe headache, and other neurological problems in Germany in 1941. By 1943, a Swedish doctor presented a paper on 142 cases, his own and from the literature.
Throughout the cataloging of European cases, the organism was undoubtedly in North America—2 of 280 mice collected from 1870 to 1919 in coastal Massachusetts would later test positive for Lyme disease. But human cases were slow to emerge, or at least to be recognized. In 1970, a Wisconsin physician, who had been tick bitten in 1968 while grouse hunting, was fortunate enough to see an astute Marquette School of Medicine dermatologist. The skin doctor remembered something from his studies: a report from 1949, in which a Swedish doctor had used penicillin on a radiating red rash. Rudolph Scrimenti prescribed antibiotics, successfully, and the hunter became the first official Lyme disease case in the United States. But in 1900s America—as in parts of it now—Lyme disease was likely mistakenly diagnosed as the flu, allergies, arthritis, signs of aging, melancholia, psychosis, neuralgia, and any of a long list of maladies that it mimics. Later it would be mistaken for other ailments as well, like fibromyalgia and multiple sclerosis.
New York State’s Long Island hugs the Atlantic coast for 118 miles from Brooklyn in the west to the dunes and bluffs of Montauk Point in the east. Here, in the region where Lyme would explode in the last quarter of the twentieth century, 136 ticks were collected in the 1940s from two oceanside locations, Montauk Point and a slip of land on the South Fork known as Hither Hills. When the specimens were tested in 1990, thirteen of them, about 10 percent, were found to harbor the Lyme bug’s genetic fingerprint. Those ticks made their home just thirty-two miles, as the crow flies, from Lyme, Connecticut. There, in 1975, two mothers would demand answers when a raft of children came down with swollen knees and arthritis-like symptoms that were later attributed to the bites of ticks and, more specifically, to a pathogen within the ticks. Yale School of Medicine became involved, and ticks were identified as the carrier, or vector, of infection.
The pathogen itself would be identified in 1981 by Willy Burgdorfer, a researcher at a US government facility called Rocky Mountain Laboratories, in Hamilton, Montana: Borrelia burgdorferi. At last, after eons of infection, sightings from Central America to the Alps, and much human suffering, the bug had a name. Europeans, too, recognized this illness. In Germany and Austria in 1996, twenty-five Ixodes ricinus ticks dating from the 1880s were dug out of institutional archives. Two tested positive for species of Borrelia linked today to Lyme disease. “Residents of Europe have been exposed to diverse Lyme disease spirochetes at least since 1884,” researchers reported, “concurrent with the oldest record of apparent human infection.” The oldest record, perhaps, but certainly not the oldest case.
A Switch, Flipped
For all the scattered human cases in 1900s Europe, Lyme disease was a long but a minor medical mystery, a small public health concern. Something happened, something coalesced, around the mid- to late-1900s to animate this millennia-old tick-borne malady. Borreliaburgdorferi-laced ticks were was no longer an atypical risk in a rare forest or field. Lyme disease was no longer the novelty of early 1900s Sweden for the dramatic red flag it bestowed on its victims. This disease grew, in the last quarter of the twentieth century, from cases measured by the handful to an epidemic infecting millions worldwide, one belatedly recognized and woefully underappreciated. To be sure, the United States began officially counting cases in 1991, meaning that doctors were mandated to report them to health authorities. Hence, some of the rise over the last quarter century can be attributed to awareness. Was this a reporting phenomenon, since we know the bug had long been in the environment? Or was this a sudden explosion that drowned out B. burgdorferi’s background noise? Could an epidemic and a phenomenon like this have been overlooked for long? This wasn’t just more cases, however; this was more ticks.
In Sweden, where some of the oldest tick data are kept, maps from before 1980 show the arachnids confined mainly to a broad but tight arc around the Stockholm archipelago; by the mid-1990s, the ticks gravitated outward into central Sweden and north along the Baltic coast. In 1995 and in 2006, Dutch authorities conducted national surveys in which they asked residents simply if they had been bitten by ticks. The per capita rate of tick bites jumped 75 percent in a decade—“a progressive threat to public health,” officials called it. Ixodes ticks have surged across the continental United States, moving from less than a third of counties in 1998 to half in 2015. In the state of Iowa, Ixodes ticks were seen in nine counties in 1990; by 2013, they had turned up in seventy-two counties, where there were clear signs this was more than a counting phenomenon. While tick numbers rose, so did the proportion infected with the Lyme spirochete, hitting a peak of 24 percent in 2013, the final year of the study. That is triple the rate of 1998.
In upstate New York, where I live, ticks are a frequent topic of conversation among long-time residents. “Do you remember seeing them 30 years ago?” a friend asked me. We agreed; we did not. I recall a large black tick in the fold of my ear after jogging through brush one day in the 1980s; this was an exotic creature indeed. By the early 2000s, all that had changed. After a late spring walk in a field around 2010, a helpful friend and I removed forty blacklegged adult ticks from my two dogs before we stopped counting. We were aghast. By then, we knew the upshot.
What flipped the switch to make this happen, in that field and in our world, were gradual, inexorable changes, long in the making, on the ground and in the atmosphere. These changes were prompted by how and where people lived, what animals they fostered and which ones they displaced, how they got around and warmed and cooled themselves, how they were fed. Human influence had become so powerful, so vast, that it exerted control over the mechanisms of weather, te
mperature, global ecology, and contagion. Lyme is listed among the giants of disease that have been and will be fueled by global climate change, including cholera, dengue, and malaria. The difference is that those are long-known agents of misery, while Lyme is new. The US Global Change Research Program predicted with “high confidence” in 2016 that a warmer world would prompt ticks carrying disease to come out earlier in spring and to move generally northward. With the same confidence, it forecasted more mosquito-borne diseases, like West Nile, a prediction outdated only months later. That was when the Zika virus—a major threat for its potential for sexual transmission and brain damage in utero—burst on the scene. Others, to be sure, lie in wait.
But Lyme disease was the first to arrive, to blossom and thrive in a wide swath of earthly territory, in the era of climate change. The US government tracks case counts as a measure of warming, along with wildfires and heat-related deaths. Lyme disease is the biggest vector-borne disease in the United States, and, when undercounting of cases is factored in, the nation’s second-leading infectious disease as well. Why Lyme disease exploded precisely when it did is not fully understood. Whether climate change prompted the epidemic or merely helped it along is an open question. But of this there is little doubt: the hand of humankind shaped this epidemic, aiding and abetting the many forces that went into creating it.
Sarah Randolph is a zoologist and Oxford University professor emeritus with close-cropped hair and a reputation that is legendary in the world of tick study. She has strong opinions on Lyme disease—“the go-to cause for any malaise,” she thinks—and a fervor for the scientific study of eight-legged creatures that bite. The “beauty” of ticks, she has written, as only a zealot can, “lies in molecular detail.” She marvels at the ingenuity of scientists who unravel their mysteries, from counting ticks on mountains to picking them off the chins of wriggling, and very unhappy, garden dormice. “Indeed fantastic!” is how she described this scientific pursuit to me. Professor Randolph’s prime focus is Ixodes ricinus, the castor bean tick, and its potential to impart tick-borne encephalitis. The world needs people like her, who love the workings and wonders of ticks, though she has been a thorn in the side of a Lyme researcher or two.
In 2010, Randolph set out to study why cases soared in three former Soviet-bloc countries of tick-borne encephalitis (TBE), a viral illness prominent in Russia and Eastern Europe. TBE can cause seizures, meningitis, and problems of thinking and memory and kills 1 to 2 percent of those infected; it is far less prevalent than Lyme disease, with perhaps 2,500 cases in Europe yearly. In 2009, cases of the disease went up in eleven of fourteen European countries, with particularly startling increases, of 45 to 91 percent, in Poland, Lithuania, and Latvia. Was this surge in disease driven by more ticks, more deer, a warming climate? No, Randolph and a colleague concluded. Instead, as incomes dropped, residents took to forests that were tick-infested to forage for mushrooms and berries or to cut wood, long-standing practices among impoverished Eastern Europeans. At the same time, the cost of vaccination against the disease—a prime tool that sharply limits cases—soared 40 percent in Lithuania, the hardest hit country with the lowest inoculation rate. This particular outbreak, Randolph maintained, was driven by poverty, unemployment, and hunger.
Randolph’s paper is one of several, cited scores of times, in which she argues that social and economic factors drive disease by putting people in the paths of ticks. She disdains buzzwords like biodiversity and is a determined naysayer of climate change as a driving factor in tick-borne disease. “Human behavioral shifts…after the fall of the Berlin wall were far more significant than climate change,” she told me.
It’s the Deer
On the other side of the Atlantic Ocean, another kind of Ixodes tick, the blacklegged tick, lives well and large in the gardens, carved-up forests, and hilly trails of Dutchess County, ninety minutes north of New York City. This tick is Ixodes scapularis, the prime mover of Lyme disease there, and it is the life’s work of another zoologist, Richard Ostfeld of the Cary Institute of Ecosystem Studies in Millbrook, New York. In 1991, Ostfeld stepped into the deciduous woods of Dutchess County in an effort to understand a plague of bug-eyed, hairy caterpillars that had defoliated vast tracts of forest. Those gypsy moth caterpillars, so numerous that poop rained audibly upon the forest floor, led Ostfeld to a discovery that would chart his course for the next quarter century. He found so many acorns that he slipped and slid on boots as if they were lined with ball bearings. The acorns, it developed, begat a bumper crop of mice. The mice, in turn, decimated the gypsy moths, feasting on the delectable shell-encased stage between crawling and flying known as the pupa. The caterpillar plague was over.
But it was what Ostfeld saw on the noses, cheeks, and ears of the mice that predicted both his future and that of an epidemic. On each mouse, there were twenty, sometimes thirty, newly hatched larval ticks, feeding on the single best mammal from which to pick up the pathogen that causes Lyme disease. Ostfeld was on a course to unravel the complex ecology of Ixodes scapularis, Borrelia burgdorferi, and Peromyscus leucopus—the tick, bug, and mouse that make up the troika of Lyme disease.
Ostfeld, a youthful sixty-something, is the senior scientist at Cary, an institute with unmowed grasses and low natural buildings that could double as a retreat center in the woods. Carved into six invisible grids, the Cary property—its flora and fauna—is also Ostfeld’s window into the life of Ixodes ticks. Ostfeld measures how many larval, nymph, and adult ticks there are in the forest and how many are infected with Lyme disease. He counts the number of ticks on shrews, chipmunks, voles, mice, and birds throughout tick season and the proportion that are infected. He looks for, and has found, other pathogens in these ticks, counting coinfections as an emerging and troubling trend in the land of ticks. He has sometimes captured an exotic or invading species, like the two Gulf Coast ticks he saw in the summer of 2016 that gave him something to watch. He has figured out which animals are “competent reservoirs” of infection, namely those likely to nurse young ticks with Borrelia-laced blood. Bite a mouse—a highly competent reservoir—and a tick is likely to be infected with the Lyme bacterium 90 percent of the time. Bite a deer, considered “incompetent,” and the tick will be infected less than 10 percent of the time.
In 2000, Ostfeld and his long-time collaborator, Felicia Keesing, introduced a groundbreaking idea into the science of disease ecology. Until then, ecosystems rich in diversity had been embraced for two reasons. They offered the promise of undiscovered substances from which to make future pharmaceuticals, and they supported animal populations key to the study of human disease. Now, Ostfeld and Keesing went one step further. A forest alive with a diverse array of wildlife, one species keeping another in check, they posited, could provide natural protection against disease. On the other hand, an ecosystem starved for diversity, the theory held, could be one in which pathogens bloomed.
The scientists’ “conceptual model,” their prima facie case of a pathogen enabled by a disordered, unbalanced environment, was Lyme disease. Devoid of predators and competitors, white-footed mice thrived in the “isolated woodlots and urbanized landscapes” of a postindustrial world, they wrote. In these diminished ecosystems, ticks feasted off the blood of the single best mammal to infect them with Lyme disease spirochetes: mice. Find an environment where mice are kept in check, one where ticks feed on animals that are not so chock full of Lyme disease spirochetes, and you will find less Lyme disease. Ostfeld and Keesing called this the “dilution effect.” The pathogen is still there in nature, as it has been for eons, but it is watered down in its ability to circulate between host and tick and, hence, to proliferate. More foxes, for example, could mean fewer mice, which could lead to fewer infected ticks. So compelling was this theory that the Ostfeld-Keesing article, in the journal Conservation Biology, has been cited some five hundred times in the seventeen years since its publication.
Sarah Randolph does not adhere to the idea that natural forces working in har
mony are, by definition, a solution for tick-borne disease. Biodiversity is a “mantra,”—“diversity protects against infection risk”—that, she has written, is “doomed to fail.” Both esteemed researchers in parasitology, Ostfeld and Randolph have, in the arcane yet amazingly feisty way of scientists, disagreed strongly in print, in a debate that hits at the core of Lyme disease theory. Forget warm and fuzzy ideas on diversity, Randolph and a coauthor argued in a pointed critique of the Ostfeld theory. Forget climate change, what they called “the other environmental bête noir” of Lyme disease. These were merely “powerful levers for attracting funding from major agencies.” Instead, blame deer: “Increased deer abundance results in increased tick populations,” wrote Randolph et al., citing a good bit of published science that agreed.
In a book called Lyme Disease, published in 2011, Ostfeld devoted three chapters to what he saw as pat explanations for the spread of tick-borne disease. They are the following: “It’s the deer.” “It’s the mice.” “It’s the weather.” Each is important, he maintained. But each, in particular deer, has been oversold. For decades, he argued, efforts have been made to tame the rise of deer in the belief that ticks would be vanquished as well. Deer were, after all, the favored host of mating, egg-laying adult ticks. No sex, no babies, no problem. In 1982, 70 percent of deer were shot on Great Island, a six-hundred-acre landmass off the coast of Massachusetts. Mice, nonetheless, were found afterward to carry the same number of ticks as before, with some indications there were even more. Researchers had better success on Monhegan Island, off the coast of Maine, where all deer were eliminated in 1999 and ticks became scarce. And after 90 percent of deer were culled in a tract of 112 homes called Mumford Cove in Groton, Connecticut, in 2000, both ticks and Lyme disease cases dropped sharply. By 2011, however, researchers took another look at the data and reported that they “did not find a statistically significant effect of the deer hunt.” Beyond this, deer travel. Controlling them on a mainland is much tougher than on an island, even if it could lessen tick populations.
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