Lyme disease - what is the real cause?

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According to the World Health Organisation, more than 30 serious new diseases have emerged in the last three decades. Mark Walters describes one of them, Lyme disease, and shows how our destruction of the environment is inextricably linked to its proliferation
 

Hunterdon County was a sleepy backwater when John Beckley arrived in 1985. Since then it has been transformed into a sprawling New Jersey suburb of more than 120,000 people. ‘I thought I was coming to a quiet rural county,’ Beckley, Hunterdon’s director of public health, told me. ‘We had an environmental staff of four, and spent most of our time inspecting or issuing permits for septic systems and wells – a dozen or so a week. Since then, my job’s gotten a lot more interesting.’

Just months after Beckley’s arrival New Jersey reported its first case of HIV. In 1986 Hunterdon County had its first cases of Legionnaire’s disease. Then in 1989 Beckley’s office began receiving reports of raccoons behaving strangely; the animals were wandering across the county’s highways and into people’s yards to attack their dogs. ‘It turned out to be the first outbreak of terrestrial rabies in the state in nearly half a century,’ Beckley said. Ten years later West Nile virus arrived.

Many of the diseases that suddenly struck Hunterdon County were not random: they were precipitated or fostered by human changes to the environment. The rabies outbreak was traced to hunters who transported raccoons from Florida and released them locally to improve hunting further north in West Virginia. Some of these raccoons were infected with the rabies virus, which marched north through the species right into New Jersey. Legionnaire’s disease, a technology-related illness, was caused when Legionella bacteria were given the opportunity to collect in warm environments provided by modern life (eg, water heaters, saunas and air conditioners), and were then aerosolised and inhaled by people nearby.

‘All these diseases were occurring against the backdrop of what has become our single biggest infectious disease problem,’ continued Beckley. That problem is Lyme disease, another disease that accumulating evidence indicates has emerged in part because of radical changes people have made to the landscape; in this case to the once comparatively stable and biologically rich forests of the eastern United States.

From mice to men

Lyme disease was first noticed in Old Lyme, Connecticut, in the 1970s, but a case wasn’t documented in Hunterdon until 1988, when 12 patients were identified. There were 30 cases in 1989, and by 1993 there were 204. Today Hunterdon County has the third highest rate of Lyme disease in the US and the highest in New Jersey. In 2000 it had more than 500 cases.

As a result of these numbers, the US health and safety agency the Centers for Disease Control and Prevention (CDC) sent a team to investigate. Beckley was one of the team’s members. The CDC concluded that one reason for Lyme’s high incidence in Hunterdon was the county’s high density of deer, which harbour the tick that carries the Lyme disease bacterium, near residential areas. Another was the high number of rock walls and woodpiles near homes. These provide refuge and breeding grounds for mice and chipmunks, which also carry the ticks. ‘Where the edge of a yard comes up against the woods, that’s an “ecotonal edge”, which is perfect habitat for ticks,’ Beckley explained. ‘That nature-culture border is where people who may be mowing the lawn or trimming branches often pick [ticks] up. Human activity has put people right at the centre of the tick’s life cycle.’

Deer and small rodents such as mice provide the literal lifeblood of the ticks. They supply not only blood meals but also a means of transportation and dissemination for the otherwise largely immobile ticks. The tick’s life cycle begins in autumn, when egg-laden females drop from the deer to the ground – frequently nestling in leaf litter for the winter. With the advent of warm spring weather, the eggs hatch and the larvae hitch a ride on mice, chipmunks or any other small mammal or bird nearby. Once on a host, the ticks feed for several days and then drop off. They develop over the next several months and re-emerge as nymphs the following spring. By then they are mobile enough to climb low-lying bushes, where they often perch at the end of a branch or leaf and wait for a larger mammal, such as a deer, to pass by. Horses, dogs or humans will do, however. It is by these poppy-seed-sized nymphs that most people become infected.

The reality of Lyme disease was brought directly home to Beckley in October 2001. ‘John and I were driving home from a weekend on Cape Cod and I started feeling this really pronounced stiffness in my spine,’ Beckley’s wife Linda told me. ‘All my muscles hurt. I lost my appetite and got very agitated. I got a fever and shivers.’ The night after a nurse practitioner had diagnosed his wife’s illness as flu, Beckley noticed a telltale bull’s-eye rash on her shoulder blade. She had Lyme disease. Mrs Beckley was cured by a three-week course of antibiotics. But she was lucky to have been diagnosed quickly. Many people don’t realise they have the disease until the symptoms are far worse. Those symptoms can include painful joint or neurological damage, and are sometimes permanent.

Driving back from the Beckleys’ after our interview, I was delayed by a traffic accident. As I waited, I reflected on a June morning several months previously when I had spent time in the fragment of old-growth woodland that is Hutcheson Memorial Forest with the forest’s director Edmund Stiles. Where, I wondered, were the world’s long, uninterrupted stretches? The intervals between major changes in our world – neighbours moving to new jobs in other cities, a mall newly constructed here, a farm giving way to a new housing development there – seem to shrink ever smaller day by day.

In a sense even the intervals of Linda’s disease had been shrunk. Her doctors had compressed the definition of her Lyme disease into the interval between when she was bitten and when she successfully completed her course of antibiotics. But this excluded the larger ecological implications of her illness and, therefore, its full meaning. Her illness was not just about a bacterium that entered her body. It was an extension of the unfortunate history of the US’s eastern forests, and it was connected to autumn oaks and hickories, an absence of predators, and an over-abundance of deer and mice. Her illness was not exclusively hers. It was an intimate part of a picture almost too big to see.

Seeing the bigger picture

Perhaps no one understands this big picture – the ecology of Lyme disease – better than Richard Ostfeld, an ecologist at the Institute of Ecosystem Studies in Millbrook, New York state. In the mid-1990s Ostfeld began to suspect he might be able to predict people’s risk of contracting Lyme disease by studying, of all things, the abundance of acorns in a region. Acorns come in bursts, or ‘masts’, with almost none produced in some years and bumper crops in others. These cycles are synchronised over large regions of the country, in part by regional weather. If acorns attract deer and mice, Ostfeld reasoned, and the incidence of Lyme disease in humans is related to the densities of these animals, the rate of human infection could be related to the production of acorns. Ecologists call this a cascade effect.

The year 1995 was a very poor one for acorn production near Millbrook, and gave Ostfeld and his colleagues an opportunity to test his theory. Millbrook is in Dutchess County, which has an unusually high rate of Lyme disease. With lots of oaks and people, it was an ideal place to conduct such a study. Ostfeld and his team measured and demarcated two sets of plots in the forest. On half of the plots Ostfeld left the poor natural acorn crop as it was. On the other plots he supplemented nature’s production with nearly a million acorns from elsewhere.

In the months that followed, Ostfeld regularly visited both sets of plots and compared what happened in the supplemented plots with developments in the acorn-poor ones. The supplemented plots attracted far more deer that autumn. The following spring, something else was evident: mouse populations had exploded in the supplemented plots; better fed, more adult mice had survived than in the unsupplemented plots and they had more young in the spring.

Ostfeld and his colleagues then dragged strips of fabric over the plots, a standard method for collecting ticks. Astonishingly, the acorn-rich plots had eight times as many newly hatched ticks, or larvae, as the regular plots. The acorns had not attracted the ticks. Rather, the greater number of deer attracted by the abundance of acorns meant that more adult ticks had dropped from the deer as they fed in the autumn. In the spring, the female ticks on the ground laid eggs, which hatched into a super-abundance of larvae by early summer in 1996.

There was something remarkable about the newly hatched larvae: they didn’t harbour the bacteria that cause Lyme disease. Even if the mother tick was infected, the bacteria were not passed through the eggs to the larvae. To become infected, a tick first had to feed on an infected animal, such as a mouse. And since almost all mice carry the bacteria, almost every tick that feeds on a mouse becomes infected.

But it stood to reason that the more mice there are in an area, the more likely it is that actively feeding ticks (as opposed to recently hatched larvae) in that area would become infected. And since more mice had been drawn to the acorn-rich plots, Ostfeld was not surprised to find a higher percentage of infected ticks there. Moreover, the higher density of infected ticks led to more Lyme disease in people. Thus, Ostfeld’s acorn theory was supported by his field experiments: acorns attract deer and mice; mice infect ticks; and infected ticks give people Lyme disease. People’s health was linked to acorn production.

The real test of Ostfeld’s theory would occur after a natural mast, however. He could then compare human infection rates in regions where bumper crops occurred with infection rates in places where they had not, or he could compare infection rates in one area over successive years. A spike in infections following a large acorn crop would lend considerable weight to Ostfeld’s theory.

The year 1997 saw one of the most prolific acorn crops in the US’s mid-Atlantic states for years. Edmund Stiles recalled the abundance of acorns in Hutcheson Memorial Forest that year. Moving through the forest, he said, was ‘like walking on marbles’. If Ostfeld’s theory was correct, the rate of infection should rise among local people in the second year after the mast. In fact, 1999 saw the third-highest number of Lyme disease cases ever reported in the mid-Atlantic region.

Why biodiversity matters

Mice and chipmunks transmit Lyme disease to more than 90 per cent of the ticks that feed on them. In contrast, possums, raccoons, birds and many other forest dwellers infect only about 10 per cent of their ticks. This goes to the heart of the ecology of Lyme disease. The greater the variety of animals there is in a forest, the smaller is the probability that ticks will feed on mice, and the chance of ticks picking up the Lyme disease bacterium is also reduced.

Severely disrupted forests can quickly lose many of their most ‘specialised’ species – animals that can’t quickly adapt to new habitats or sources of food. ‘Generalists’, on the other hand, often accommodate change. While specialised species vacate disrupted forests, resourceful generalists, such as deer and mice, often expand their numbers.

Ostfeld wondered whether this meant that the loss of species in the US’s north-eastern forests, which now favour generalists such as mice and chipmunks, had contributed to the increase in Lyme disease. Conversely, if a greater variety of species was returned to a forest, would that reduce the density of mice and chipmunks, and, therefore, the prevalence of the Lyme disease bacterium among ticks and people? Would a greater degree of biological diversity, in other words, offer people a certain degree of protection from Lyme disease?

Ostfeld couldn’t recreate the rich and diverse forests of old, but he could test his so-called dilution theory with computer modelling. He created a computerised forest. Each time he added a new species to the computer-modelled forest, the density of ticks infected with the Lyme disease bacterium declined.

Ostfeld and his colleagues tried to get a real-world grasp of his hypothesis by listing all the eastern US bird, mammal, and lizard species (from Florida to Maine) on which ticks carrying Lyme disease are known to feed. Ostfeld’s researchers then compared the numbers of different species within regions along the US’s eastern seaboard with the rates of Lyme disease in people living in those areas. They found that the areas with more species had fewer cases of Lyme disease per capita. High biological diversity, it seemed, did tend to minimise the rate of Lyme disease infection in the human population; at least that was one reasonable interpretation of Ostfeld’s findings.

In considering how to lower the risks of Lyme disease, many more ecological questions need to be answered. Ostfeld is now trying to understand, for example, the effects of habitat fragmentation on Lyme disease risk for people. What animal species are our strongest allies in protecting us from Lyme disease? And just how big need a forest patch be for it to support many species and, therefore, lower the risk of Lyme disease?

The ecology of Lyme disease reminds us that the connections between the earth and human health are ancient. Changes in forests and their species, Ostfeld’s research suggests, are reflected in human disease. Places such as Hutcheson Memorial Forest are touchstones of tranquillity in a world undergoing constant human-driven change. We will probably never know if Lyme disease afflicted forest dwellers there 500 years ago, but the diverse ecology at that time would have weighed against its doing so. If the Lyme disease bacterium were present, the indigenous forest dwellers might, over millennia, have developed immunity to it.

What we can be sure of is that in our short-sighted efforts to make the world more hospitable for humans we have also been making it more hospitable for many of the microbes that cause disease.

Mark Walters is the author of Six Modern Plagues: and how we are causing them (Shearwater Books, 2003)

This article first appeared in the Ecologist February 2004