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Dirt is your friend

Modern life has taught us that all bugs are bad news and should be killed, but our obsession with hygiene is damaging the microbial marvels that protect us from disease

The Sunday Times
Stories that dirt may be good for us have been circulating for some years, but the truth is very complicated
Stories that dirt may be good for us have been circulating for some years, but the truth is very complicated
JOHN RENSTEN/GETTY

“Fighting the germ of our near obsessive cleanliness,” reads the headline from the Mumbai Mirror, dated December 2015. Followed by: “Making your house too clean can be dangerous for your children. Sterility, it seems, comes at a price.”

“I attach,” says Professor Graham Rook of University College London, who has emailed me the clipping, “a self-explanatory image. That article, particularly appearing in a newspaper in Mumbai ... is a ghastly misunderstanding of the situation that might well result in deaths.”

Mumbai is city of 18m people, almost half of whom live in slums. It is, like any crowded, impoverished city, a paradise for pathogens, the bugs that cause human disease. To tell these people not to keep their houses clean is to sentence many of them to death.

Nevertheless, there is science behind the idea, possibly the most important medical science of our time. Stories that dirt may actually be good for us and excessive hygiene may be making us ill have been circulating for some years. The idea is, first, that we need to be infected by bad bugs so we can build up resistance and, second, that we need to be infected by good bugs that keep us healthy. Both of these are true, but it’s an abuse of science to say we should just wallow in dirt. This is what makes Rook angry. “Everything,” he says, “gets wildly overinterpreted.”

The idea that infections may be good for us was originally named the “hygiene hypothesis” (HH) by Professor David Strachan, an epidemiologist at the University of London, in a paper published in 1989. Strachan was trying to explain the increase in hay fever and asthma in the 20th century. He thought this may be due to lower levels of infections in early childhood. Bugs were being cleaned up and allergies were increasing as a result.

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Similar observations had been made since the 19th century, but Strachan gave the idea a name and a headline — allergies were increasing explosively. One of his key suggestions was that smaller family sizes were reducing bug-sharing among children.

For the next three decades, Strachan’s tentative idea generated a dangerous popular mythology. The word spread that our modern hygiene fetish was a mistake: it compromised our ability to fight allergies and disease. We should, it was thought, dirty things up a bit. This was dangerous because hygiene — combined with antibiotics — has saved billions of lives.

Germ warfare: Dr Martin Blaser has found that antibiotics are weakening our defences
Germ warfare: Dr Martin Blaser has found that antibiotics are weakening our defences
JOAO CANZIANI

“Is it better,” asks Dr Molly Fox, a biological anthropologist at the University of California at Los Angeles, “to have your children get cholera rather than an allergy? That’s a weird question — the idea that we should send our children to play in mud or they shouldn’t wash their hands is a very dangerous reaction to this hypothesis.”

Nevertheless, HH has stuck in the popular imagination, not least because it contains a grain of truth. But it is complicated. Very. We don’t yet know exactly what that truth is. What we do know is that it involves somewhere between 30 and 300 trillion bugs that you carry around with you. This teeming mass weighs about three pounds and it is known as your microbiome.

The microbiome is a 500m-year-old inheritance. It would have appeared in our first vertebrate ancestors; we still probably carry many of their bugs. Anything that has been around that long must serve some useful purpose. But, somehow, from the 19th century onwards, we concluded all bugs were bad and must be killed.

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The reality is that only a few hundred bugs are actually harmful. Millions more either live harmlessly inside us or keep us alive and healthy. We have no idea how many. In one experiment, faecal samples from two subjects yielded 174 species never before seen in the human gut and 31 new species. There are probably millions more.

But the inhabitants of the modern world decided to declare war on all bugs, friendly or not. They did so with medicine, primarily antibiotics, and huge changes in lifestyle.

We had smaller families, which reduced beneficial cross-contamination. We moved away from the country, losing the good bugs that float in rural air and severing contact with animals. One comparison of Hutterite and Amish communities in America showed the Hutterites had much more depleted microbiomes — they permitted the use of farm machinery, whereas the Amish only use animals and were healthier as a result. We lived more indoors, again losing the benefits of the bugs in fresh air. And, yes, we became obsessively clean. We also dosed ourselves with antibiotics at every opportunity.

The list of afflictions thought to be linked include type 1 diabetes, inflammatory bowel conditions, depression and Alzheimer’s

In the process, we suppressed many terrible diseases — polio, smallpox, measles, plague, cholera and so on. But, somehow, we acquired many more, perhaps not as lethal, but terrible nonetheless. Along with the huge increase in allergies, type 1 diabetes simply exploded. Diabetes is thought to kill 5m people a year and the horizons of survivors are shrunk by the necessity of lifelong treatment.

Linked to that, obesity is now an epidemic, as are the host of life-changing and life-threatening conditions that come under the heading of metabolic syndrome.

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The list of contemporary afflictions thought to be linked to our microbiomes includes most autoimmune diseases such as type 1 diabetes, inflammatory bowel conditions, coeliac disease, Graves’ disease, Crohn’s disease and so on. Mental illnesses, especially depression, are high on that list, as is Alzheimer’s. Crucial work by Fox has found population-level evidence of a link between increased hygiene and Alzheimer’s. But, she warns, this requires a great deal of research to be confirmed.

This transformation in the pattern of disease has marched in lockstep with the changes in our microbiomes in the contemporary world.

Dr Martin Blaser is the director of the Human Microbiome Project at New York University and author of a very lucid and alarming book — Missing Microbes: How the Overuse of Antibiotics Is Fueling Our Modern Plagues. The book is one shock after another, but at its core is this simple statement: “Recent studies suggest that some otherwise normal individuals have lost 15%-40% of their microbial diversity and the genes that accompany it.” We are, in short, increasingly defenceless.

“What we have known for decades,” he tells me, “is that the healthy microbiota protects us against the invaders. But what happens when the microbiota gets depleted? People will be more susceptible to invaders.

“The second point is that we live in a world that’s smaller, we’re all interconnected, we’re only days away from any village in the world and we also have a world with a lot of antibiotic resistance. So we have all the pieces of a perfect storm.”

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Fox also points out that pathogens such as zika and ebola are much more dangerous as a result of natural selection — antibiotics mean pathogens evolve resistance, and living more indoors will increase the opportunities for more virulent strains. “Pathogens that kill their hosts can perpetuate in those circumstances. Pathogens that kill human hosts quickly wouldn’t have been as successful in premodern conditions.”

This is the central point. It means we will need to preserve hygienic habits, but in a much more targeted way. We will need to distinguish between good and bad dirt.

In his book, Blaser foresees an “antibiotic winter” in which we have no defences against new plagues to match the Black Death or the great flu pandemic of 1918-19, which killed tens of millions. Blaser’s belief that antibiotics are the most crucial factor in the destruction of our microbiomes is not universally shared, though no one doubts its importance.

“In type 1 diabetes, we don’t really have good enough data to back it up,” says Dr Tim Tree, an immunologist at King’s College London and a type 1 sufferer himself. “There are a couple of reports that suggest early antibiotic use isn’t a good idea ... I certainly think it’s likely to be one of the driving factors that affect microbiome diversity in the gut, and that impacts your immune system, and that impacts type 1 diabetes.”

So what is to be done? Again, it’s complicated. In his immaculate Islington house, Graham Rook is covering A4 sheets with diagrams and illegible handwriting. As his email about the Mumbai Mirror showed, he loves to explain his work in compendious and exact detail.

There’s something like a doubling of the risk of type 1 diabetes if you’re born by c-section

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A microbiologist, in 2003 Rook came up with a new hypothesis that went some way beyond the HH. He called it the “old friends hypothesis” (OFH). By friends, he means the creatures that have accompanied and helped humans through life; by old he means ancient — bugs and worms that go back hundreds of millions of years. These are the key inhabitants of our microbiomes.

There are three groups of friends. There is the familiar bacterial and viral mass forming the microbiome; then there are helminths, tiny parasitic worms that we can probably do without; and, finally, there are the bugs we pick up from the environment.

These last are very important and not enough noticed. If you end up in the sterility of intensive care, your microbiome will deplete because you are not in contact with the normal teeming zoo that just floats around in the air. After you get out, it will, probably, restore itself. But it won’t if you’re old and in a poor-quality care home where you barely leave your room. Microbiome depletion may, in fact, be one of the leading killers of the elderly. In general, if you feel better in the countryside than in town, it’s because your bug population is happier and more diverse.

The HH was based on the idea that the childhood infections we had suppressed provided protection against allergens. The OFH disputed this. “Strachan’s was a perfectly logical assumption,” says Rook, “but a whole lot of epidemiological studies were done very quickly after that, which showed things like measles and so on do not protect you from allergic disorders. In fact, not only were childhood infections not protecting you from allergic disorders, some were actually provoking them.”

Measles, plague and the like are known as “crowd” infections — the bugs only thrive above certain levels of population density. Measles seems to have been unknown until the later years of the Roman Empire. Crowd infections became epidemic in the great move into the cities during the 19th century. So they could not be the protectors the HH suggested they were; something much more ancient must be involved.

But how to nourish these ancient friendships? The first big point is, don’t fall for the idea that depleted microbiomes always recuperate. Usually they do, but often they don’t. The effects of the loss of bug variety are cumulative, and Blaser points out that experiments with mice suggest it might be passed down generations. Especially don’t fall for this idea with very young children. There are all kinds of studies showing antibiotic treatment during the first year is linked to later disease — notably type 1 diabetes.

Yoghurt is delicious, but Blaser knows that, even when loaded with probiotics, it’s not doing his microbiome any good. In fact, all the people I spoke to pointed out that none of the probiotics currently sold has been tested, so forget that.

Diet, however, is crucial. Rook scribbles two graphs, one showing a flat line with several sharp peaks. This is the immune system acting normally, doing nothing and then launching a swift attack on an invader. His next graph shows a flat line at a higher level with no peaks. This is metabolic syndrome, in which the immune system never turns itself off, causing a permanent state of inflammation. You get it by eating junk food and depleting your microbiome, and it will probably kill you. No backsliding — eat a varied diet with a lot of fibre.

Avoid unnecessary medication. Don’t use antibacterial soap — it doesn’t do anything except, perhaps, promote resistance in bad bugs. Antibiotics go off like bombs in your microbiome. In adulthood, it should recover and treatment may be necessary. But if it isn’t — say, you have a cold or other viral infection — then taking antibiotics is socially irresponsible: it spreads resistance in pathogens. Try to avoid giving them to children, but be careful, they may be life-saving. The big medical intervention to avoid if you can is a caesarean section.

“There’s something like a doubling of the risk of type 1 diabetes if you’re born by c-section,” says Tim Tree. C-sections are now commonplace, accounting for more than a quarter of births in the UK. The long-term effect on the human microbiome is incalculable, but it will be huge.

Microbiomes are transmitted down the generations not by genes but by infection. At birth, a baby is coated with the vaginal and anal bacteria of the mother. This gives it a fabulously complex dose that is the start of a healthy microbiome. Babies born by c-section only receive skin bacteria and, as a result, are at greater risk of autoimmune disease. Not only is type 1 diabetes increasing, it is being contracted at a much earlier age — c-sections may be the reason.

So beware caesareans, but if you do have one, go for a swab. This involves wiping vaginal mucus over the baby. It seems to work, if only incompletely.

Do not pursue every potential cure that attracts publicity. Faecal transplantation has become — for obvious reasons — famous. It does, indeed, work very well for patients with a Clostridium difficile infection. C diff is a potentially lethal bug found in faeces; it often spreads in hospitals. Transplanting somebody else’s poo into your intestine has definitely worked in cases. It causes an invasion of good bugs that wipe out the C diff. Don’t, however, get too enthusiastic and try this at home. Rook points out it all depends on the poo, so donors should be chosen with great care.

Finally, there is the matter of hygiene. This is a balancing act. “If your child is helping you in the kitchen and has just pulled the guts out of an unprepared chicken,” Rook explains, “she definitely needs to wash her hands thoroughly. But if she’d just been playing out in the garden and got a little bit of soil on her hands, I wouldn’t worry about it.”

It’s also generally agreed that if your baby’s dummy is dropped on the floor, you shouldn’t rush to sterilise it. Rather, clean it by putting it into your own mouth. This will help the transfer of your microbiota to your baby, a crucial process.

And, on the subject of soil, get out into the fresh air, preferably in the countryside. The belief that greenery is restorative is literally true: it repopulates your microbiome. As well as the bugs in your gut, they are also on your skin and in your airways. Rural fresh air is good for all of these and, crucially, sets up mechanisms within the airways that inhibit allergic responses.

That’s about it. For now. Once we have worked out who our old friends are, then we can dose babies immediately after birth. But that is some time off. We are at a very tricky moment, caught between the need to stave off the old killers and disablers and the urgency of preventing the new ones.

Human survival will always be a full-time job. We are temporary arrangements of biological matter in the midst of an ocean of living creatures, whose depths we have only just begun to imagine.

And this ocean flows through us. It is full of many old allies and a few sociopathic enemies, many of which have sprung to life because of our modern misconceptions and bad habits. There is no way back, but we have at least learnt to shake hands with our most ancient and best friends.