Eating off the floor: How clean living is bad for you

Ten steps to a healthier life and more wealth through embracing the bacteria around you.

The Slightly Longer than Five Second Rule.

Book titles are difficult to choose. In theory, a perfect title is concise, compelling, enticing and, oh by the way, accurately conveys some aspect of the book?s contents. In practice, most titles involve more compromise than perfection. The working title of my first book was Unknown. The book was about the biological unknown and what remains to be discovered as told through the stories of the discoverers and would-be discoverers. I liked the title. It seemed to capture some essence of what I was up to and offered a good conversation starter. People would ask what I was doing and I would say ?oh, going to spend the afternoon in the Unknown.? The editors were not so sure. One day I received an email forwarded from someone within my publishing house that said, ?when is Dunn going to decide on a title?? At first I did not understand and then it became clear. The cover page of my book read, ?Title: Unknown.? I got the point. The book became Every Living Thing.

The working title of my new book was Clean Living is Bad for You. This title had the advantage of offering a simple thesis. It also seemed more family friendly than the alternative suggested by my neighbor, ?People Who Like it Dirty are More Healthy.? In six words, Clean Living is Bad for You set forth the thesis that living a life that was too clean and devoid of other species makes you sick. I imagined a cover with a kid licking cookies off of the floor beside a neat freak father holding antimicrobial wipes. The father would have a textbox over him that read, ?sick? and the kid would have her own textbox reading ?healthy.? Inside, you would find ten quick steps to immersing yourself in more kinds of bacteria and, in doing so, living a healthier life with more wealth through embracing the bacteria around you¹.

But then I started to write the book and discovered the Clean Living title no longer captured what the book was about. I suppose in such a moment there are two options. Stick with the simple title, which might be easier to sell, albeit not representative of the book, or give in to the complexity. I gave in to the complexity, hundreds of millions of years of complexity. I wrote about the influence of our changing relationship with other species in general?including the bacteria on our bodies and in our houses, but also the predators in our gardens, pathogens everywhere and crops and cows in our fields?on our health and well being. The title became ?The Wild Life of Our Bodies, predators, parasites, and partners that shape who we are today,? which was not quite what the book was about either, but closer.

I changed the title because the book changed. But there was also another issue. I wasn?t sure if the idea that clean living is bad for you was true. We know less about bacteria and clean (or dirty) living than I expected, much less.

In a coarse way, dirty living is good for you and clean living is bad for. You are part bacteria, if you got rid of the life on your skin or in your gut, you would almost certainly die. But, what I had envisioned was an expansion of the slightly more complex idea called the hygiene hypothesis, whose argument goes something like this? Humans moved from rural lifestyles outdoors to hyper-clean lifestyles indoors in city apartments with central air, sealed windows and surfaces scrubbed clean, at every opportunity, with antimicrobial wipes. That transition led us to spend less time getting ?dirty? outside. It also ?cleaned up? many of the species we need around us indoors that would allow us to get dirty with life. This combination prevented many of our immune systems from developing normally². As a consequence, our immune systems tend to get ?messed up? when we live in cities. They revolt against us in the form of asthma, allergies, Crohn?s disease, inflammatory bowel disease and, depending on who you ask, maybe even MS and autism. In other words, clean living of one sort or another may be at the root of the majority of modern, chronic, diseases.

The hygiene hypothesis is simultaneously elegant, sweeping, important, vague, and poorly tested. Very little is known about how a change in the bacteria you are exposed to might negatively affect your immune system (though that is rapidly changing as more and more scientists study the problem). Even less is known about how microbes vary with human lifestyles. When nothing is known, many things can seem plausible. The early days in any field like household microbiology are simultaneously delightful and frustrating, a kind of Wild West in which everyone is armed with ideas and ready to shoot.

Is that a Worm in My Colon??Some things have been tested. It has been shown that the presence or absence of worms in the gut of someone can influence their immune system. Taking worms away from someone with worms can make them more likely to suffer from autoimmune diseases. Conversely, adding them back can make them less likely to suffer from autoimmune diseases. Just how worms affect our immune systems is not yet clear, but that there have been negative consequences of getting rid of our worms, at least for some people, is becoming clear. That said, we lost our worms because we started using indoor plumbing and walking around in shoes. When people talk about getting back to nature and being less hyperclean they seldom mean pooping near other people?s feet and hands. The same public health systems that got rid of our worms also save lives, by preventing the transmission of other pathogens, such as Cholera, via that same route. But there is more than a worm at the bottom of this story.

If the hygiene hypothesis were right, we might expect the composition of bacteria and other microscopic species on individuals or in houses to vary as a function of our lifestyles and our health should vary, in turn, as a function of the composition of those microbes. The good news is, this prediction is very testable.

How would you do the study? One approach would be to sample the microbes in houses in rural and urban areas and then, from those same houses, ask individuals about their health and wellness, particularly as relates to immune disorders (I?m not quite there yet, but see footnote four when you get to it). The hygiene hypothesis doesn?t really specify whether it is the diversity (how many kinds), composition (which kinds) or abundance (how many in total) of tiny life forms that matters. You could measure all three. It would be relatively easy, albeit not cheap.

Personally, my guess is that whatever the result is, it is likely to be dependent on other factors. It seems unlikely that urban living in Rio de Janeiro means the same thing as urban living in, say, New York, in terms of exposures to different numbers and types of microbe species. The climate is different. The other species present (e.g., birds, bats, pets and insects) are different. It also seems as though even within an urban environment buildings are likely to differ as a function of their architecture, design, and building materials. Or at least one hopes that how you make a building influences who lives in it. Pigeons prefer to nest in vertical structures. Houses with attics are better for bats. But what we know tends to be about animals, and even then, mostly the animals with backbones. What about the microbes? Someone needs to study how they vary as a function of how and where we live. Fortunately, someone did, sort of.

In December of 2011, Steven Kembel, a research associate at the Biology and the Built Environment Center at the University of Oregon, and colleagues published a study in which they compared the microbial composition of hospital rooms that differed in how they were designed. Anyone who has stayed in one knows hospital rooms are not homes and yet the rules that apply to hospital rooms might also apply to homes. After all, the cleanest among us seem to want to make our homes ?hospital clean.? I?ve seen the advertisements, you are supposed to scrub and scrub until even the children shine.

The modern, ?sterile,? hospital room, with Kembel?s sampling devices and standardized ?open window,? installed.

If the hygiene hypothesis is right or even on the right path, what Kembel and crew would expect to see would be that those design elements that make the hospital rooms more like a rural house, more natural in some crude sense, should be more likely to favor a diversity of ?good? microbes. Conversely, they might expect that the features that make the rooms more sealed off and ?modern,? cleaner if you will, should favor pathogens and disfavor the full richness of other species, that wealth I mentioned earlier.

Is there Life in There??This is a good moment to point out what is obvious to microbiologists but not to the advertising agencies who tell us to kill the germs, namely that it is not possible to kill ?the germs.? The world is dense with other species. Every inch of every thing around you right now is covered in living cells, cells that make do with what you leave them. Your only choice in terms of how you affect these other species, this universal, shimmering, majority, is a choice of which of them to favor and which to disfavor. Microbes happen. There are even bacteria species capable of ?consuming? Triclosan, the active ingredient in antimicrobial soaps, wipes and underpants. We live among the microbes much as we live among the molecules (and microbes) in air. And so what Kembel chose to ask was not whether there are bacteria in hospital rooms. Yes, there are. They are on the patients, on the walls, on the children?s books in the waiting room and even on the doctors and nurses. What matters is not whether there is life in there, but which life is in there, which is precisely what Kembel sought to study².

The experimental component of Kembel?s study focused on one aspect of the rooms, whether or not they were vented by standard AC/Heating systems or by windows. Half of the rooms were assigned to one of each of these categories. This was the only factor Kembel and crew varied, but they measured many other features of the rooms, much in the way you might measure additional variables when comparing old and young rain forests, variables like humidity, temperature and wind. When they did, Kembel and colleagues found that the diversity and abundance of bacteria varied as a function of the design of the rooms. BOOM. BIG RESULT. OK, well, wait, the overall result was not so surprising, but there is more, there is the issue of why they varied.

Clean living is Bad for Diversity?Kembel and friends³ found the composition of bacterial communities ?in window-ventilated patient rooms? to be ?intermediate between mechanically ventilated patient rooms and outdoor air.? Open the window, the lesson seems to be, and both air and microbes come inside. What was more, when rooms ventilated using windows were warmer and drier, they tended to be more like the mechanically ventilated rooms suggesting that it might be, in part, the warmth and dryness of the mechanically ventilated rooms that helps to keep them ?different.? These differences in composition were also associated with differences in diversity, the number of kinds of bacteria. The outdoor air was most diverse, followed by rooms with an open window and then, finally, rooms that were mechanically ventilated.

Put it together and it appears the more dry, warm and sealed off a room is the fewer kinds of bacteria it is likely to have. This is exactly what the hygiene hypothesis would predict, or really it is more like what the hypothesis assumes but tends to avoid testing, that the conditions in which we try to envelope ourselves, warm rooms with the windows closed and the central air turned on, lead to the lowest diversity of microorganisms in our surroundings. And what the hygiene hypothesis argues is that while we may tend to think of this as a hygiene success story, it represents failure. This lower diversity may lead our immune systems to develop in such a way as to be unable to make full sense of the world. This aspect of ?clean living? may well be bad for us. More needs to be tested and yet Kembel?s results are exciting, a suggestion that our air conditioned/heated, closed off apartments and offices all around the world may be devoid of diversity, a diversity we might need for our bodies to make sense.

Staphylococcus aureus. It may be beautiful, but it is also one of the species Kembel et al. classified as bad news

Clean Living is Good for Pathogens?Somewhat buried in this paper is another revelation, one that is quieter but, if true, perhaps even more novel. In addition to considering the diversity of benign and/or even good bacteria associated with the environment in general, the paper also evaluated the abundance, or a measure of abundance anyway, of bacteria closely related to human pathogens. The abundance of these bacteria varied among rooms but not simply as a function of how they were ventilated. The best predictor of the number of these potentially bad species was the room?s diversity of bacteria. Rooms with a greater diversity of bacteria had fewer individuals of the bacteria species similar to human pathogens. The diversity of bacteria explained (accounted statistically for) more than half of all of the variation in the number of potential pathogens!

Could the diversity of good bacteria in some rooms actually be reducing the density of bad bacteria? There is precedent for such an idea, though it comes from grasslands rather than hospitals or bedrooms. In grasslands and other outdoor habitats (Grasslands are an appropriate example for Kembel, who started off studying grassland diversity before moving on to hospital rooms), an enormous body of literature considers whether more diverse grasslands are harder for an invading life form to take over. The answer?though I will admit to summarizing a literature that includes hundreds, maybe thousands, of papers in six words? is, yes diversity helps to resist invasion. In those fields, diverse grasses efficiently use the resources invaders need, preventing them from gaining a foothold. Could having a diversity of bacteria in your home or hospital room not only make your immune system more likely to develop normally but also help to outcompete the bad news bugs in the first place? YES, YES, YES, the answer is definitely maybe⁵.

A Better Title in 55 Words or Less?All of this brings me back to the issue of my book title. I think it is possible we will find that clean living leads us to live alongside fewer rather than more bacteria species and that this really is bad for you, for more than one reason. But for now the nuanced title, the title that captures the gist of what we do and don?t know is something like ?Scientists may have discovered that Clean Living is Bad for You. The idea is supported so far by the data, but key tests have not been done and it is important to point out that really dirty living is bad for you too. Really dirty living gives you Cholera. Scientists agree you don?t want that.?

Maybe if the publisher chose a small enough font, it would work. Or maybe not.

Table of evolutionary contents: Here you can skip ahead or backward to the other chapters in the story of how we came to depend on or ignore other species during our evolution, whether they be those about the cow, the chicken, the hamster, bacteria (on Lady Gaga, on feet, in bathrooms, as influenced by antimicrobial wipes, as probiotics, in the appendix), pigeons and urban gardens, house sparrows (to be published next week, stay tuned), predators, diseases, dust mites, basement dwellers, lice, field mice, viruses, yeast, the fungus that produces penicillin, bedbugs, houseflies, and more.

Or for the big picture of how I think these stories come together to make us who we are, check out The Wild Life of Our Bodies.

Footnotes

1?I would, of course, have pointed out early in the book that the wealth in question was not economic but rather the richness of microbial diversity, the living wealth of the sort that really does grow on trees and also on you. I swear, I would have pointed it out early.

2?S.W. Kembel, E. Jones, J. Kline, D. Northcutt, J. Stenson, A.W. Womack, B.J.M. Bohannan, G.Z. Brown, and J.L. Green.2012. Architectural design influences the diversity and structure of the built environment microbiome. The ISME Journal. doi:10.1038/ismej.2011.211

3?I don?t know if they are all friends. They might hate each other, but one can only say ?and colleagues? so many times and even ?colleagues? implies, rightly or wrongly, that they are collegial.

4?There are advantages and disadvantages to being a scientist who also writes rather than a full time science writer. The disadvantage is that if I have a really great story about a crazy scientist who does crazy things (and boy do I have some) you probably can?t tell it because it might be the person who ends up voting on your tenure or reviewing your papers. The advantage is that when you write about something that is really interesting, you can go back to your lab and announce to everyone, ?hey, guess what we are going to study.? So it was that I announced to my lab, earlier this year, ?hey, part of what we will be studying is whether or not clean living is bad for you?and we are going to do it by letting people do science in their own houses about their own lives!? The broad project is called your wild life, though I don?t mind saying that wasn?t the title we started with.

The folks in my lab and I, along with Holly Menninger and Steve Frank, both also at North Carolina State University, and a whole tribe of scientists from the Nature Research Center have now teamed up with Noah Fierer and his crew (friends) at the University of Colorado Boulder, to do a bunch of fun things none of us could have imagined doing on his or her own⁶. Among them is a big study to sample the life, including but not exclusive to the microscopic life, in thousands of houses across North America. All of this is possible because we are enlisting citizens?you, your cousin, that other cousin no one talks to with the house that doesn?t have running water and your mom?to sample their own houses and, for a subset of more ambitious folks, collect data on the climate, and other habitat characteristics of their houses, from fridge to toilet rim. We want you to help us go boldly where few have gone before, into your bedroom. Wait, that didn?t sound right, but you get the idea.

We already have thousands of people signed up, people to whom we are sending sampling kits, but we will keep sampling until the money runs out because the more houses we are able to sample the more we will be able to tease apart how different elements of how you live (your air conditioning, your pets, your houseplants and even the size of your house) influence what species you live with, so please sign up and hopefully we will be able to get to your house too and in the meantime you can read about our progress and fun, whether or not your house has been sampled and participate in our other related studies about the life in your house, be it bacteria, ants, or crickets. Our goal is to sample enough houses that we can figure out what makes some houses rich in good (or at least benign) bacteria, fungi, pollen and even insects and others abundant in fewer species, some of them pathogens and dangerous pests. In the process, we want to engage people in being able to study their own lives, where big mysteries lurk (albeit sometimes in small bodies). We think part of the story will be climate, part will be urbanization and part will be just how houses are designed (which would be great, because it then allows us to think about how to better design homes), but we could be wrong. We are wrong all the time. That is the thing about writing and science. The story, no matter what its title, doesn?t always lead quite where you think it might. With any luck, it goes somewhere far more fun.

I love my job. The truth is, this story has already taken a fun turn, even before we have gotten the first results back about bacteria, fungi, archaea or pollen. We have already been wrong, in a way. We began our wild life project by asking citizens to tell us about the species in their houses. In doing so, we discovered that a mysterious, hopping, lunging, insect species no one knew was widespread is thriving in basements throughout North America. Is it in your basement, let us know by filling out a survey here.

5?The big caveat in this part of the story has to do with the issue of what it means to be a bacterial species ?related to? a pathogen. Because Kembel and colleagues identified bacteria species based on relatively few of their genetic letters, it is easy to know who belongs in what clan, but any given clan is likely to have some wonderful folks and some outlaws. The genus Staphylococcus includes terrible, terrible, pathogens such as MRSA that can kill. It also includes the teddy bear of a species, Staphylococcus epidermidis, which lives all over your body and probably does you a fair number of favors, if you know what I mean. Well, what I mean is that it is a normal component of most human bodies and may even help to defend us against truly bad species, such as closely related pathogens. What all of this means is that the species Kembel calls similar to pathogens are similar, but might or might not be pathogens. What is needed as follow up is a study in which more of the nucleotides of the species present in the rooms are studied to conclusively separate outlaws and teddy bears. OK, that analogy has been taken too far, but the point is what Kembel offers here is not resolution but, instead, a clearly articulated version of a hypothesis with preliminary data, which is what I meant when I said, ?maybe.?

6?I know, technically this is a footnote to a footnote. Welcome to my brain. But I wanted to point out two more people are also now involved in helping to make this big project a reality. Holly Menninger was recently at a meeting where, to the sound of fiddle music, she may have convinced Jonathan Eisen to help make the kinds of projects the citizens working with us can do more sophisticated (imagine identifying the bacteria in your house yourself at home) and Jason Bobe to help make the answers we get related to human health more relevant.

Images: Eating Kix off the floor: Chris and Jenni on Flickr; Hospital room with vent to the out of doors (Photo by Steven Kembel); Staphylococcus aureus: Microbe World on Flickr.

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